Advisory Committee On The Microbiological Safety of Food

ACMSF A3 Listeria Elderly:ACMSF A3 cover 27/7/09 9:32 PM Page 1
Advisory Committee on the

Microbiological Safety of Food
Ad Hoc Group on Vulnerable Groups
Report on the Increased Incidence

of Listeriosis in the UK
Crown copyright
Published by Food Standards Agency Advises the Food Standards Agency on the
July 2009 Microbiological Safety of Food
FSA/1439/0709
Further copies of this publication can be downloaded from: acmsf.food.gov.uk/acmsfreps/


Advises the Food Standards Agency on the

Acknowledgements
The Ad Hoc Group wishes to thank the people listed at Annex I and the
Secretariat for their assistance.
The ACMSF accepts full responsibility for the final content of the report.
Ad Hoc Group on Vulnerable Groups Report on the Increased Incidence of Listeriosis in the UK
Contents
Subject Paragraph
Summary 19
Definition of a vulnerable group 79
Chapter 1: Introduction 1.1 1.7
The ACMSFs approach to its work 1.5 1.7
Chapter 2: Hazard identification and characterization 2.1 2.28
Background 2.1 2.5
Listeriosis in pregnancy 2.6 2.8
Listeriosis in non-pregnant individuals 2.9 2.13
Virulence of L. monocytogenes 2.14 2.15
Epidemiology of listeriosis and changing pattern of 2.16 2.21
human listeriosis in England and Wales
Conclusions 2.22 2.26
Recommendations 2.27 2.28
Chapter 3: Report rationale 3.1 3.6
Chapter 4: Consideration of key hypotheses to 4.1 4.64
explain the increase in listeriosis cases
Hypothesis 1: The rise in cases of listeriosis in compromised 4.1 4.6
people over 60 years of age is an artefact associated with
improved case recognition
Hypothesis 2: The population predominantly affected by 4.13
the recent increase has become more susceptible to
infection with L. monocytogenes
Changes in medical practice which may render the elderly at
increased risk of listeriosis
Treatment of haematological malignancy 4.14 4.16
Management of solid organ malignancies 4.17
Statins 4.18
Disease modifying anti-rheumatic drugs (DMARDS) 4.19
Antisecretory Agents 4.20
i
Non-behavioural factors which may increase 4.21

susceptibility to gastro-intestinal infection (and
pathogens whose sole/primary portal of entry is
the gastro-intestinal tract
Immunosenescence 4.22
Malnutrition 4.23
Other measures of increased susceptibility
to listeriosis in the elderly 4.24
Hypothesis 3: The pathogen L. monocytogenes has 4.30 4.33
become more virulent and new strains are better
able to cause bacteraemia
Conclusions 4.34
Recommendation 4.35
Hypothesis 4: Levels of exposure have increased 4.36 4.37
Listeria in foods 4.38 4.47
Social factors food handling and 4.48 4.53
consumption patterns
Chapter 5: Risk management 5.1 5.34
Legislative limits
European limits 5.1 5.7
US limits 5.8
Food industry controls 5.9 5.18
Consumer Advice 5.19 5.24
Chapter 6: Summary of Conclusions 6.1 6.41
and Recommendations
Annex I: List of organisations and contributors who assisted the Group
Annex II: Terms of reference and Membership
Annex III: Analysis of consumption patterns in the over-65 age group
List of Tables and Figures
Glossary of Terms and Abbreviations
References
ii
Summary
1. In this report the Ad Hoc Group has considered the change in

epidemiology of human Listeria monocytogenes infection in the UK
characterised by increased incidence of listeriosis from 2001.
2. This report follows information from the Health Protection Agency to

the Advisory Committee on the Microbiological Safety of Food (ACMSF)
which indicated that the incidence of listeriosis in England and Wales in 2005
remained higher than pre-2001 levels. In Scotland in 2005 the incidence was
also significantly higher than in 2004 and from the period 1993 to 1999. A less
pronounced increase in incidence was also reported in Northern Ireland. The
disease occurred predominantly in older patients and presented as
bacteraemia in the absence of CNS infection.
3. In June 2007 ACMSF referred this issue to its Ad Hoc Group on

Vulnerable Groups for consideration as a priority. The Group met on six
occasions over a period of 16 months to assemble information and review
evidence relating to diagnosis, typing data, artefacts, case histories, social
factors, changes in consumption habits and cumulative risk factors and to
inform the development of ACMSF advice to the Food Standards Agency.
4. The Group set out several possible areas of activity to try to identify the
cause of the change in epidemiology in the over 60s age group as a series of
hypotheses. These were subjected to challenge. They considered information
on the bacterium Listeria monocytogenes including its survival, virulence and
behaviour in food and the food chain. The epidemiology of the bacterium was
reviewed including transmission and trends in listeriosis in the UK, EU and other
countries. UK data on human L. monocytogenes sub-types in relation to food
exposure history and comparison with food isolate typing data were also
examined. Blood culture and sampling trends in the general population,
including the elderly, were discussed and changes in clinical assessment in the
over 60s were also considered. Other areas of investigation included
surveillance of L. monocytogenes in foods, shelf life, changes in chilled food
production and food safety controls. The Group also examined social and
behavioural factors in the over 60s age group including data on consumption
patterns, consumer purchasing, storage and food handling behaviours. Other
factors affecting vulnerable groups were explored including underlying medical
conditions and changes in their care. Risk factors and underlying assumptions
to assess whether the target population had become more susceptible to
L. monocytogenes were evaluated, and UK and international consumer
guidance on the risks posed by L. monocytogenes were reviewed.
1
5. Key conclusions and recommendations arising from the work of the

Group were:
The majority of cases of human listeriosis appear to be sporadic

and foods associated with transmission are predominantly ready
to eat, with extended (usually refrigerated) shelf life capable of
supporting growth of L. monocytogenes. The reported increase
in listeriosis since 2000 in the UK and some European countries
has occurred almost exclusively in patients aged over 60 years
presenting with listerial bacteraemia. However, there is no
evidence for a common source relationship between these
changes in presentation of listeriosis. Pan-European surveillance,
epidemiological and microbiological investigations are
recommended to investigate these changes in listeriosis in
different Member States and to ascertain whether there are
common generic or risk factors occurring in the UK and other
countries. Studies to develop screening methods for
L. monocytogenes isolates are also recommended to investigate
differences in virulence and differences between isolates from
different patient groups and time periods.
The increase and shift in presentation of listeriosis cannot be

attributed to improved diagnostics, as a comparative increase has
not been reported in L. monocytogenes isolated from blood
cultures from patients with CNS infections or pregnancy-
associated cases. Similarly, levels of bacteraemia associated with
other foodborne pathogens have not increased in the over 60s.
To take account of any under-reporting of estimated cases of
L. monocytogenes in the UK, work is needed to investigate and
reduce the incidence of listeriosis in the over 60s. The
ascertainment ratio for human listeriosis should also be
estimated. Routine collection of denominator data for selected
medical investigations associated with listeriosis infection would
inform work to analyse infection trends and our understanding of
changes in epidemiology associated with this organism.
Elderly individuals are more likely to have underlying conditions

which predispose to listeriosis than younger age groups. The
increase in cases of listeriosis associated with the over 60s cannot
solely be attributed to the general demographic increase of this
age group in the population. The rate of listeriosis has increased
three-fold in the over 60s from the early 1990s to the present. It
is recommended that work is undertaken to investigate whether
the management of underlying conditions in these age groups
has contributed to the rise in listeriosis. Retrospective studies
2
and data collection should be conducted to identify which

underlying conditions are most associated with listeriosis in this
age group and UK infection surveillance should incorporate data
on denominator populations and numbers of medical
investigations undertaken (including blood cultures).
Maintaining active surveillance for Listeria spp. in foods is

important to inform control of this organism. Such surveys should
examine a wide range of foods (shopping basket surveys) and
account for food purchases at catering and retail outlets.
Data on shopping and food behaviour and consumption patterns

in the over 60s is limited. More information on the food
consumption and food handling and storage behaviours in the
home of this age group, including those who are vulnerable, is
needed to inform factors contributing to the risk of listeriosis. In
the absence of such information it is recommended that general
consumer food safety advice should be developed and
communicated to the over 60s (including those in vulnerable
groups), as well as to those who prepare and provide their food
and those who provide medical advice about the risks of
listeriosis to these groups. Studies should be carried out to
evaluate the impact of such advice on these groups. It is also
recommended that the FSA refers this Report to its Social
Science Research Committee to consider the food behaviour,
storage and handling practices of elderly people in the home.
The food industry has implemented many controls over the past
two decades to prevent the contamination of foods with
L. monocytogenes and the principles of food safety management
are well established in the food industry. Evidence suggests that
the incidence and levels of this organism at the points of
production and sale are not higher than those detected in the
late 1980s. The Group was unable to assess whether an increase in
shelf life across chilled commodity areas or the development of
new foods could account for an increased risk of listeriosis as
limited information was available. However, the Group received
Ad Hoc information from one supermarket chain that indicated
that there had been no recent marked increase in the shelf-life of
chilled foods. Therefore the Group was unable to assess whether
an increase in shelf lives across chilled commodity areas or the
development of new foods could account for an increased risk of
listeriosis. It is recommended that any future advice to industry
and enforcement authorities reiterates the importance of
temperature and shelf life control, hygiene/cleaning and
formulation of food in preventing contamination or limiting the
3
growth of L. monocytogenes in foods. The Committee also

reiterates its advice that FSA should work with the food industry
to ensure that formulations including salt levels of specific
products are not changed without considering the impact of
these changes on microbiological safety.
The organism has been found in chilled ready-to-eat foods at a

low level which probably represents a low risk provided storage
time and temperature conditions are maintained at appropriate
levels prior to consumption. The provision of durability
instructions such as 'use by' dates on some perishable foods sold
loose was found to be variable. One survey in the North West of
England found use by information to be more common on retail,
sliced, cooked meats from supermarkets (74%) than market stalls
(6%); delicatessens (8%) or butchers (7%). Therefore it is
recommended that the FSA reviews the need for consistent
advice on such products.
6. The assessments made and the conclusions reached by the Group
reflect evidence, oral and written, drawn from the scientific community,
industry, government departments and Agencies, EFSA and the scientific
literature. The Groups conclusions and recommendations are brought
together at the end of the report.
Definition of a vulnerable group

7. For listeriosis, vulnerability is considerably increased within the following
groups: elderly (i.e. people more than 60 years of age, regardless of whether
they fall into other groups below) cancer patients, patients undergoing
immunosuppressive or cytotoxic treatment, unborn and newly delivered
infants, pregnant women, diabetics, alcoholics (including those with alcoholic
liver disease) and a variety of other conditions. Rarely, infection can occur in
patients without any known risk factors.
8. Although risk factors for listeriosis are well documented, identification

of specific vulnerable groups, with the exception of pregnant women, is not
straightforward. Immunocompromised individuals are acknowledged as being
vulnerable to listeriosis, but the term is ill defined a problem exacerbated by
the use of other terms such as immunodeficiency. Indeed, many standard
texts (Donnelly and de Pauw, 2005) do not attempt to define the term
immunocompromised, although in other settings, for example, prevention of
severe infection following exposure to varicella zoster virus,
immunocompromised is defined in detail (Anon, 2006).
4
9. A definition of a vulnerable group, such as the elderly, is necessary if

public health initiatives designed at reducing the risk of listeriosis are to be
directed to those individuals (or those responsible for their care) in the most
effective manner. Yet there is no accepted definition of elderly or other
similar terms such as older adult. NHS Direct states, for example, that older
people are at risk of listeriosis1. Better definition of at-risk groups would also
serve to raise awareness of listeriosis among healthcare professionals caring for
the elderly, particularly those with patients with additional risk factors such as
underlying co-morbidities such as malignancy and autoimmune disease,
especially those receiving immunosuppressive therapy (Mulley, 2008).
1 NHS Direct web site: http://www.nhs.uk/conditions/Listeriosis/Pages/Introduction.aspx
5
Chapter 1: Introduction
1.1 In September 2005 and December 2006, the Health Protection Agency
(HPA) alerted ACMSF Members to a change in the epidemiology of human
L. monocytogenes infection in England and Wales. This change was
characterised by an increase in the numbers of reported cases from 2001,
which occurred predominantly in patients of 60 years of age and over, who
presented with bacteraemia (the presence of bacteria in the blood) without
central nervous system (CNS) infection. This increase, which represented a
doubling in reported cases since 2001, occurred in most regions in England and
Wales, in both genders, and could not be explained by outbreaks recognised
during this time.
1.2 In Scotland in 2005, the incidence of listeriosis was significantly higher
than in 2004 and the period 1993-1999. Furthermore, the clinical presentation
in Scotland in 2005 was similar to that observed in England and Wales, with the
disease occurring predominantly in older patients with bacteraemia in the
absence of CNS infection. No significant increase was observed in Northern
Ireland up to 2005. However, an increase was reported in 2006-07. Additional
data were presented, which suggested that the altered epidemiological/clinical
picture in England and Wales was not artefactual.
1.3 In June and December 2007, HPA confirmed that the increase in
listeriosis had continued into 2007. Similar increases had also been reported in
other European countries, including France and Germany. Following the
introduction of a standard structured surveillance questionnaire for listeriosis
in 2005, sufficient data were accrued for preliminary analysis. Initial
investigations showed significant differences in the exposure histories of
patients infected with different subtypes of L. monocytogenes. Separate
analysis of data from routine reference typing of isolates from food indicated
associations with the same or similar food types. From these findings it was
hypothesised that specific food types gave rise to infection with specific
L. monocytogenes sub-types.
1.4 In June 2007, ACMSF considered the high level of reporting of listeriosis
in the UK. The Committee agreed that the change in epidemiology was more
likely to be linked to social factors, including changes in dietary/food
behaviour and food production rather than changes in the bacterium. It also
identified a series of data gaps and issues requiring detailed consideration
including diagnosis, typing, case histories, changes in consumption habits, and
cumulative risk. The Committee referred this issue of listeriosis in the elderly
to its Ad Hoc Group on Vulnerable Groups for further discussion as a priority2.
2 This Group was set up to examine potential microbiological safety risks to vulnerable groups including
the elderly; and to define vulnerable groups in relation to foodborne disease, review key hazards,
consider food consumption and behaviour patterns and to provide advice to these groups.
6
The ACMSFs approach to its work
1.5 The Ad Hoc Group met six times (over a period of 16 months) to
consider documentary and verbal evidence relating to listeriosis in the elderly.
To frame the scope of our deliberations we examined a series of hypotheses
to establish the cause of the rise in listeriosis. Key issues for consideration
included the validity of the increase, susceptibility of the target population
and exposure levels. To investigate these hypotheses, we considered
information on L. monocytogenes, including its survival, virulence and
behaviour in food and the food chain. The epidemiology of the bacterium was
reviewed, including transmission and trends in listeriosis in the UK, EU and
other countries. Blood culture and sampling trends in the general population,
including the elderly, were discussed and changes in clinical assessment in the
over 60s were also considered. Other areas of investigation included
surveillance of L. monocytogenes in foods, shelf life, changes in chilled food
production and food safety controls.
1.6 We also examined social and behavioural factors in the over 60s,
including data on food consumption patterns. Other factors affecting
vulnerable groups were explored including underlying medical conditions and
changes in vulnerable groups care. Risk factors and underlying assumptions to
assess whether the target population had become more susceptible to
L. monocytogenes were evaluated and UK, EU and international consumer
guidance on the risks posed by L. monocytogenes were reviewed.
1.7 It should be noted that the report uses the terms over 60 and the
elderly interchangeably. Where ages other than over 60 are used in this
report (i.e. over 65) these relate to ages defined and used in specific data or
studies that were considered by the Group.
7
Chapter 2: Hazard identification and

characterization
2.1 Listeria is a genus of Gram-positive bacteria and comprises six species:

L. monocytogenes, L. ivanovii, L. innocua, L. welshimeri, L. seeligeri and L. grayi.
Listeriosis is the disease caused by L. monocytogenes, although very rare cases of
infection in humans due to L. ivanovii and L. seeligeri have also been reported. In
other animals, most cases are due to L. monocytogenes but with 10-15% due to
L. ivanovii (McLauchlin 2005).
2.2 Listeria monocytogenes can be categorised using a number of different
phenotypic and genotypic methods: the former have been now largely superseded
by the latter. The most common methods currently used are molecular serotyping
(based on the characterization of genes encoding or co-transcribed with the
serotype antigens, Doumith et al, 2004) and amplified fragment length
polymorphism analysis (AFLP, Guerra et al, 2002). Selected isolates can be
characterised by pulsed-field gel electrophoresis (PFGE, Graves and Swaminathan
2001). These methods do not directly generate information on the virulence of
individual isolates.
2.3 Complete genome sequences are publicly available for several different
L. monocytogenes strains, as well as other Listeria species (Glaser et al, 2001; Nelson
et al, 2004). There is now a considerable body of information available on the use
of various animal and cell culture models, which have identified genes associated
with the virulence of L. monocytogenes (Vazquez-Boland et al, 2001): most of
which encode cell surface structures or secreted products. However, there is less
information on polymorphisms, which occur naturally within these virulence genes
and which might affect the ability of this bacterium to cause infection.
Consequently tools for routine screening of L. monocytogenes isolates for
differences in virulence are not available.
2.4 Listeriosis occurs in a wide variety of animals, as well as humans, and most
often affects the placenta, the central nervous system or the bloodstream.
Amongst farm animals, listeriosis is most often diagnosed in sheep, cattle and goats.
In humans, serious infection is most often recognized. Although subclinical
infections do occur they are rarely identified (McLauchlin 2005).
2.5 In humans, infection is most often recognised in the immunocompromised,
the elderly, pregnant women and unborn or newly delivered infants. Case-fatality
rates of 2040% or greater occur, dependent upon the patient group infected
(Table 1). Cases can be classified as two groups; those associated with pregnancy
(the pregnant or newly delivered women, the unborn or newly delivered infant) as
well as the non-pregnant (McLauchlin 2005).
8
Table 1: Mortality rates in selected outbreaks of systemic listeriosis

Year Country Cases Mortality Food
(deaths) rate vehicle
1980-81 Canada 41 (18) 44% Coleslaw
1983 USA 49 (14) 29% Milk
1983-7 Switzerland 122 (34) 29% Soft cheese
1985 USA 142 (48) 34% Soft cheese
1992 France 279 (63) 23% Pork tongue
in aspic
1998-9 Finland 25 (6) 24% Butter
1999-2000 France 26 (7) 27% Pork tongue
in jelly
2000 USA 29 (7) 24% Turkey meat
Adapted from Bell and Kyriakides. Listeria, 2nd ed, 2005, Blackwell.
Listeriosis in pregnancy
2.6 Maternal listeriosis occurs throughout gestation, but is rarely detected
before 20 weeks. The mother is usually well with a normal pregnancy but may
have mild symptoms (chills, fever, back pain, sore throat and headache and,
sometimes, conjunctivitis, diarrhoea or drowsiness) or be asymptomatic until
the delivery of an infected infant. Symptomatic women may have positive
blood cultures. Underlying pathologies or immunosuppression have not been
identified as risk factors for pregnancy-associated listeriosis (McLauchlin 2005).
2.7 With the onset of fever, foetal movements are reduced, and premature
labour occurs within about 1 week. There may be a transient fever during
labour, and the amniotic fluid is often meconium-stained and discoloured.
Culture of the amniotic fluid, placenta or high vaginal swab (HVS) post delivery
invariably yields L. monocytogenes. Fever in the mother resolves soon after
birth and the HVS and faeces are usually culture-negative within 1 month. While
the outcome of infection for the mother is usually benign, that for the infant is
more variable and can be fatal or have long term sequelae in those that survive.
Abortion, stillbirth and early-onset neonatal disease occur and probably reflect
the gestation stage of exposure and/or infection. Maternal infection during
pregnancy but without infection of the foetus can even progress to placental
infection without ill effects for the foetus (McLauchlin 2005).
2.8 Neonatal infection usually presents as early (less than 2 days after
delivery), or late (more than 5 days old) onset disease. Early neonatal listeriosis is
predominantly a septicaemic illness, contracted in utero or during labour. Late
neonatal infection is predominantly meningitic and can be associated with
hospital cross-infection, contact with the post-natal environment or possibly
9
from the mother during delivery. Early onset disease represents a spectrum of
mild to severe infection, which can be correlated with the extent of
microbiological invasion: those most severe having invasion of the blood, central
nervous system or internal organs. Neonates who die of infection usually do so
within a few days of birth and have pneumonia, hepatosplenomegaly, abscesses
in the liver or brain, peritonitis and enterocolitis. Diagnosis of early onset
neonatal infection is by culture of blood and CSF as well as swabs from
superficial sites, gastric aspirates, and meconium. Diagnosis of late onset
infection is made by blood or CSF culture (McLauchlin 2005).
Listeriosis in non-pregnant individuals

2.9 Listeriosis in infants older than 1 month is very rare, except in those with
underlying disease. In adults and juveniles the main syndromes are central
nervous system (CNS) infection, or bacteraemia. Most cases occur in the
immunocompromised, but about one-third of patients with meningitis and
around 10% with primary bacteraemia are immunocompetent. A wide range of
risk factors are associated with listeriosis and these include; cancers,
autoimmune disease, treatment with immunosuppressive agents, alcohol-
related disease, and diabetes mellitus (McLauchlin 2005).
2.10 The clinical presentation of meningitis is the same in all groups, but
progression is more rapid in immunocompromised subjects. Gram stains of CSF
deposits can be negative, and the clinical features of infection are such that it
is not possible to distinguish between listerial meningitis from that due to other
infectious agents. Diagnosis is by culturing CSF or blood (McLauchlin 2005).
2.11 Primary bacteraemia presents with a spectrum of severity with fever
and other non-specific signs of infection. Rarer manifestations of listeriosis
include arthritis, hepatitis, endophthalmitis, cutaneous lesions, and peritonitis
in patients on continuous ambulatory peritoneal dialysis, endocarditis, and
pneumonia. Diagnosis is almost always achieved by culture of blood or other
clinical material (McLauchlin 2005).
2.12 Foodborne outbreaks of acute gastroenteritis with fever have been
described. The foods associated with these outbreaks have been diverse, but
heavily contaminated by the bacterium. Large numbers of L. monocytogenes
are present in the stool and may also occur in blood in cases of severe
infection. The ability to cause gastroenteritis may be specific to certain strains
of L. monocytogenes and this presentation has not been recognised in all
foodborne outbreaks (McLauchlin 2005).
10
2.13 The numbers of cases with a fatal outcome increases with age (Table 2).
Table 2: Reported deaths amongst non-pregnant listeriosis cases in

England and Wales 1990-2007
Death of patient (% of cases)
Age Group Yes No Not known Total
0-9 2 (10%) 17 (81%) 2 (9%) 21
10-19 5 (16%) 26 (81%) 1 (3%) 32
20-29 4 (12%) 25 (76%) 4 (12%) 33
30-39 17 (22%) 39 (50%) 22 (28%) 78
40-49 29 (21%) 91 (66%) 18 (13%) 138
50-59 73 (27%) 152 (57%) 43 (16%) 268
60-69 151 (32%) 269 (57%) 48 (10%) 468
70-79 226 (37%) 308 (51%) 69 (11%) 603
80+ 207 (44%) 211 (45%) 48 (10%) 466
Unknown 8 14 23 45
Total 722 1152 278 2152
Source: HPA unpublished data
Virulence of L. monocytogenes
2.14 Various animal and cell culture models have been developed to study
the virulence of L. monocytogenes (Vazquez-Boland et al, 2001). Most of these
have been based on either rats or mice or intracellular growth within
mammalian cells growing in vitro. Non-human primate models have also been
described. Some models bypass the intestines by injecting the bacteria into
the peritoneum or blood, whilst others have used the oro-gastric route.
Except for primates, these models do not include the complete foodborne
route of exposure and are poor at investigating differences in virulence
relevant to food-borne listeriosis. However, there is some evidence from them
(together with that from epidemiological observations) that suggests that
there are naturally occurring avirulent or virulence-attenuated strains:
phenotypic and genotypic tests are not routinely available to characterise the
expression of all virulence genes (see next paragraph) or identify differences in
virulence. However for public health purposes, all L. monocytogenes, including
those present in food, should be regarded as potentially pathogenic
(McLauchlin 1997).
11
2.15 L. monocytogenes is a facultative intracellular pathogen, and multiple

genes have been identified, which allow this bacterium to adhere to, invade
and move within and between mammalian cells. Such genes include those
which encode for proteins which are: cell surface-associated (internalins)
involved with adhesion and induction of phagocytosis; secreted and involved
with dissolving intracellular membranes and allowing the bacterium to escape
into the cell cytoplasm (two phospholipases and a haemolysin); interacting
with the host-cell cytoskeletal components and allowing intracellular mobility
(actA protein; Vazquez-Boland et al, 2001).
Epidemiology of listeriosis and changing pattern of human

listeriosis in England and Wales
2.16 Consumption of contaminated food is believed to be the principal
route of infection and common source outbreaks, together with sporadic
cases, occur. Infection can also be transmitted, albeit rarely, by direct contact
with the environment, infected animals or by cross-infection during the
neonatal period. The majority of cases are/appear to be sporadic. Foods
associated with transmission are predominantly ready-to-eat, with extended
(usually refrigerated) shelf-life, capable of supporting the growth of
L. monocytogenes. Foods associated with transmission world-wide are shown
in Table 3.
Table 3. Food products associated with the transmission of listeriosis

worldwide
Dairy Meats Fish Vegetables Complex

products foods
Soft cheese Cooked Fish Coleslaw salad Sandwiches
(Raw) milk chicken Shellfish Vegetable
Ice cream/ Turkey Shrimps rennet
soft cream Frankfurters Smoked fish Salted
Sausages mushrooms
Butter Cod roe
Pt and Alfalfa tablets
rillettes Raw vegetables
Pork tongue in Pickled olives
aspic Rice salad
Sliced meats Cut fruit
(melons)
Hummus
Source of data from case and outbreak reports in the world literature. Wagner and McLauchlin.
Biology in Handbook of Listeria monocytogenes. CRC Press, Boca Raton. 2008. pp3-25.
12
2.17 After the rise in cases in England and Wales associated, at least in part,
with the consumption of pt between 1987-9 (McLauchlin et al, 1991), the
annual totals of reported cases declined during the 1990s to between 87 and
128 per year. However, since 2000 the annual number of listeriosis cases
reported increased to 146 and 136 cases in 2001 and 2002 respectively, and to
182-237 cases from 2003-2007. Cases associated with pregnancy, with central
nervous system infection and in people aged less than 60 years remained at
similar levels. An increase in reports has occurred, almost exclusively in patients
aged over 60 years with bacteraemia (Fig. 1; Gillespie et al, 2006). This increase
is independent of demographic changes in the population and has resulted in
an approximate tripling in the rate of the disease in those aged 60 years and
over. In England and Wales: 3.3-4.7 cases per million were reported in 1990-1992
compared with 13.2 in 2007 (Fig. 2). A similar increase is observed when
considering the total numbers of blood cultures and CSF specimens from
which L. monocytogenes was isolated (Fig. 3). It is also of note from this Figure
that the numbers of CSF specimens yielding L. monocytogenes has remained
essentially the same since 1990.
Fig. 1. Numbers of reported listeriosis cases:

CNS = central nervous system infections.
Bact = bacteraemia in the absence of CNS infection.
Source: HPA
13
Fig. 2. Age specific rates of listeriosis in England and Wales 1990-2006
Source HPA
Fig. 3. Total L. monocytogenes isolations from blood and CSF
Source HPA
2.18 The rates of listeriosis have considerably increased in all groups aged 60
years and over, and show an increased rate with increasing age (Fig 4).
14
Fig. 4. Age group specific rates of human listeriosis in England

and Wales
Source HPA
2.19 The proportion of cases in patients aged 60 years and over without
underlying illnesses was not significantly different before or after 2000. Of all
patients aged 60 years and over, 9% had no reported underlying illness for the
period 1990 - 1999, and 6-14% for 2000 - 2007 (Table 4).
Table 4. Numbers of cases with and without underlying illnesses in all

patients 60 years and over
Numbers of cases (%) aged 60 years and over
Year With underlying No underlying Not recorded
condition condition
1990-1999 383 (70%) 50 (9%) 115 (21%)
2000 53 (79%) 7 (10%) 7 (10%)
2001 68 (73%) 6 (6%) 19 (20%)
2002 70 (74%) 10 (10%) 15 (16%)
2003 102 (73%) 18 (13%) 19 (14%)
2004 65 (45%) 9 (6%) 71 (49%)
2005 76 (62%) 7 (6%) 40 (32%)
2006 93 (73%) 12 (9%) 22 (17%)
2007 124 (81%) 21 (14%) 7 (5%)
Source: HPA unpublished data
15
2.20 Whilst small outbreaks were recognized between 1999 and 2007, in
association with consumption of hospital sandwiches, butter and sliced meats
(Table 5), these represent a small proportion of the total number of cases and
do not explain the overall increase. The increase in those aged 60 years and
over was due to multiple strains of L. monocytogenes and occurred in all
regions.
Table 5. Cases and clusters of human listeriosis in England and Wales
1999-2007 and associations with food vehicles3
Year Region Cases Vehicle

1999 NE England 4 Hospital sandwiches
2003 NE England 17 Butter
2003 NE England 18 None identified
2003 S Wales 2 Hospital sandwiches
2003 SW England 5 Hospital sandwiches
2004 E Mids 6 None identified
2004 SE England 2 Hospital sandwiches
2005 NW England 1 Sliced meat
2006 London 1 Sliced meat
2007 London 1 Hospital sandwiches
Source: Gillespie et al 2006 and HPA unpublished data
2.21 A similar change in incidence of listeriosis has been reported in Scotland

and Northern Ireland (ACMSF 2006, ACMSF 2007a, ACMSF 2007b) and in
Germany (Koch and Stark, 2006). The rise in cases in Germany occurred
together with changes in surveillance and raised diagnostic awareness
(listeriosis became a notifiable disease in 2001) and resulted in a more than
doubling of the numbers of reported cases between 2001 and 2005. The
increase in cases in Germany occurred almost exclusively in patients aged
60 years and over and did not appear to be linked to any single common-
source outbreak: the cases overall were predominantly sporadic in nature.
Significant increases in cases were also reported in Belgium, Denmark, France,
Lithuania, The Netherlands, and Spain (Denny and McLauchlin, 2008). There is
no evidence for a common source relationship between these changes which
have occurred in the UK with those in other countries.
3 All food vehicles contaminated with the same type of L. monocytogenes as infected the patients.
16
Conclusions
2.22 Human listeriosis is a rare but serious disease which occurs most often
in patients with cancer, those undergoing immunosuppressive or cytotoxic
treatment, the elderly (over 60 years of age), the unborn and newly delivered
infants, the pregnant woman, diabetics, alcoholics (including those with liver
disease) and a variety of other conditions.
2.23 Consumption of contaminated food is believed to be the principal

route of infection and common source outbreaks together with sporadic cases
occur.
2.24 The majority of cases are/appear to be sporadic and foods associated

with transmission are predominantly ready-to-eat, with extended (usually
refrigerated) shelf-life, capable of supporting the growth of L. monocytogenes.
2.25 Since 2000, the annual number of listeriosis cases reported has
increased and the increase has occurred almost exclusively in patients aged
over 60 years with listerial bacteraemia. This increase is independent of
demographic changes in the population and has resulted in an approximate
tripling in the rate of the disease in those aged 60 years and over in England
and Wales: 3.3-4.7 cases per million were reported between 1990-1992 and 13.2
cases per million in 2007. However the degree of under-reporting of listeriosis
in the UK has not been recently estimated.
2.26 A similar change in presentation of listeriosis has been reported in

Scotland and Northern Ireland and Germany. Significant increases in cases
were also reported in Belgium, Denmark, France, Lithuania, The Netherlands
and Spain. There is no evidence for a common source relationship between
these changes which have occurred in the UK and those in other countries.
Recommendations
2.27 Pan-European surveillance and epidemiological and microbiological
investigations should be used to investigate changes in listeriosis in different
Member States and to ascertain if there are common generic or risk factors
occurring in the UK with those in other countries.
2.28 Studies should be undertaken to develop methods for screening

L. monocytogenes isolates for differences in virulence and investigate the
differences between isolates from different patient groups and time periods.
17
Chapter 3: Report rationale
3.1 This report focuses on our efforts to try to identify the cause(s) of the
recent increase in L. monocytogenes cases in the over 60s. We chose to
examine a series of four hypotheses. These are shown below together with
brief details.
Our four main hypotheses
1. The rise in cases of listeriosis in immunocompromised people over

60 years of age is an artefact associated with improved case
recognition.
2. The population predominantly affected by the recent increase has

become more susceptible to infection with L. monocytogenes.
3. The pathogen, L. monocytogenes has become more virulent and

new strains are more capable of causing infection which manifests
as bacteraemia in this group of patients.
4. Levels of exposure have increased.
(1) The rise in cases of listeriosis in immunocompromised people over

60 years of age is an artefact associated with improved case
recognition
3.2 We considered the possibility that the recent rises in listeriosis in

England and Wales were an artefact. Thus are we now detecting infections
previously missed because either patient management and/or laboratory
testing protocols for the diagnosis had changed?
(2) The population predominantly affected by the recent increase has

become more susceptible to infection with L. monocytogenes
3.3 One possible explanation for the recent increase in cases is that
the population predominantly affected by the recent increase,
immunocompromised people over 60 years of age, has become more
susceptible to infection with L. monocytogenes. We thus reviewed evidence
to determine whether the changes in treatments available to treat conditions
more common in the over 60s could have had the side effect of increasing
vulnerability to L. monocytogenes infection.
(3) The pathogen, L. monocytogenes has become more virulent and

new strains are more capable of causing infection which manifests
as bacteraemia
18
3.4 It is known with other foodborne pathogens such Salmonella spp. that
bacteria can vary in their virulence attributes. We therefore examined the
hypothesis that the strains of L. monocytogenes responsible for the recent rise
in cases in the over 60s have virulence properties that are different from those
identified in strains isolated from past cases.
(4) Levels of exposure have increased
3.5 Another possible explanation for the rise in cases of listeriosis in the
elderly is that their exposure to the organism has increased as a result of
increased contamination of foods, changes in processing and composition of
foods, or changing patterns of consumption, or food storage in the over 60s.
To examine this hypothesis, we received and reviewed evidence on food
contamination levels with the pathogen and the frequency of
L. monocytogenes-positive samples. We also reviewed available data on food
purchase patterns, particularly those relevant to the groups with potentially
increased risk of L. monocytogenes infection.
3.6 These hypotheses will be considered in the following chapter.
19
Chapter 4: Consideration of key hypotheses

to explain the increase in listeriosis cases
Hypothesis 1: The rise in cases of listeriosis in

immunocompromised people over 60 years is an artefact
associated with improved case recognition
4.1 The increase in cases of listeriosis associated with elderly age groups
cannot be attributed to the general demographic increase of this age group in
the population alone. However the elderly are becoming an increasing
proportion of the population (16% of the UK population were aged 65 and over
in 2006, compared with 13% in 19714). Furthermore, the increase in over 65s is
about to undergo a marked acceleration over the next two decades. In 1991
there were approximately 9 million over 65s in the UK and in the following
10 years this increased to approximately 9.4 million (in 2001). By 2006, the
numbers had increased to 9.7 million and it is estimated that this will be
followed by a marked increase in over 65s, reaching approximately 10.5 million
by 2011 and nearly 12.75 million by 2021. It is therefore especially important to
understand the factors contributing to the increase in listeriosis in the group.
Since this report was prepared the ACMSF has been made aware of an increase
in the incidence of campylobacteriosis in the over 60s age group (ACMSF, 2009).
4.2 The surveillance of listeriosis in England and Wales is passive and such
systems are prone to both under-ascertainment and pseudo-outbreaks
following increased interest in the public health community. Although
reporting artefacts cannot be excluded, no increased interest in listeriosis from
2000 onwards has been detected and reporting and referral patterns of
individual laboratories could not be identified (Gillespie et al, 2006).
4.3 Improvements in laboratory methods (especially in the isolation of

L. monocytogenes from blood) or changes in local clinical practice (e.g. more
detailed investigations of patients with acute febrile illness presenting to
primary care) might explain the increase in cases diagnosed or the altered
clinical presentation.
4.4 The majority of diagnostic microbiology laboratories in the UK utilise

one of a small number of commercial automated systems for blood culture.
There have not been any changes in detection technologies that we believe
would affect ascertainment of bacteraemia cases. All of the systems would
readily support the isolation of L. monocytogenes.
4 http://www.statistics.gov.uk/cci/nugget.asp?ID=949
20
4.5 The national increase in the number of reported cases of bacteraemic

listeria infection in older patients coincides with increased recognition of age
discrimination in healthcare (Scott, 2000). A national director of older peoples
services was appointed for the NHS in England in November 2000 with a mandate
to reduce ageism in healthcare (Anon 2000a). Subsequently the NHS launched a
national plan in 2001 to ensure older people receive the same treatment as those
under 65 (Kmietowicz, 2001). As a result of these initiatives, it is possible that the
intensity of investigation of sepsis in the elderly has increased. However, other
studies have challenged the extent of ageism in NHS healthcare and the practical
impact of age discrimination is uncertain (Hubbard et al, 2003).
4.6 If there was a significant increase in the proportion of elderly patients with
sepsis undergoing blood culture, at least some of the change in listeriosis
epidemiology might be artefactual. National data are not routinely available on
the number of blood cultures collected stratified by age group. However, data
from a large Scottish diagnostic laboratory indicated that although there had
been a steady increase in blood cultures submitted from 2000-2007, there did not
appear to be any relative increase in the proportion of such samples submitted
from patients over the age of 60.
Conclusions
4.7 L. monocytogenes will grow on most non-selective media; therefore
improvements in microbiological media would be unlikely to increase the
diagnosis of listeriosis (McLauchlin 2005). Although the introduction of
mandatory reporting of meticillin-resistant Staphylococcus aureus bacteraemia in
England in 2001 has led to an increase in blood cultures being taken, this is
insufficient to explain the increase or shift in presentation described here (Anon
2000b, Anon 2005b). Further evidence that the increase was not due to improved
diagnostics is provided by the absence of a significant increase in the isolation of
L. monocytogenes from blood cultures from patients with CNS infections or
from pregnancy-associated cases (Gillespie et al, 2008). In addition, there has not
been an increase in bacteraemia caused by other foodborne pathogens (i.e.
Salmonella and Campylobacter) in the over 60s. (Gillespie et al, 2008).
4.8 The degree of under-reporting of listeriosis in the UK has not been

estimated recently. An ascertainment ratio of 2 (estimation of the numbers of
cases of illness to the numbers reported to national databases for laboratory
confirmed infections) for human listeriosis was estimated by Adak and
colleagues (Adak et al, 2002). The amount of under-reporting (ascertainment
ratio) for human listeriosis could be estimated by comparing the numbers of
cases reported to national databases with the numbers of cases ascertained in a
subset of diagnostic centres. Since the highest numbers of cases occur in those
60 years old and over and there is a possibility of surveillance artefact due to
changes in diagnostic procedures having introduced bias, resources should be
concentrated on investigation of incidence in this section of the population.
21
4.9 The Second Infectious Intestinal Disease Study will not address this
problem. However, even if significant under-reporting of listeriosis has
previously occurred, the FSA has recently estimated that L. monocytogenes is
responsible for the highest numbers of deaths due to a food-borne pathogen
(FSA 2007, Annual report of the Chief Scientist 2006/7). Since the highest
numbers of cases occur in those 60 years old and over, resources should be
concentrated to reduce the incidence in this section of the population.
4.10 Our ability to analyse infection trends and understand changes in the
epidemiology would be enhanced by the routine collection of denominator
data for selected medical investigations associated with infection.
Recommendations
4.11 The amount of under-reporting (ascertainment ratio) for human
listeriosis should also be estimated.
4.12 UK surveillance of infection should be enhanced to incorporate data

on the corresponding denominator populations, including numbers of
relevant medical investigations, such as blood cultures, undertaken.
Hypothesis 2: The population predominantly affected by

the recent increase has become more susceptible to
infection with L. monocytogenes
4.13 Demographic changes in the population might have resulted in an over-
representation of cases from particular age groups without a true increase in risk.
Life expectancy in the UK is increasing; therefore an increase in listeriosis in older
patients is likely to occur. However, calculations controlling for the changing age
structure in England and Wales during the surveillance period generates a
consistent increase in risk amongst those aged 60 years and over in both sexes
and in most regions. The risk of listeriosis increases with each successive age
group (Fig. 4). Medical advances have resulted in the UK human population
surviving for longer with chronic conditions (Anon 2005a) with a likely increased
susceptibility to listeriosis. Whilst it has not been possible to obtain suitable
denominator data required to examine such changes in detail, it is unlikely that
they would result in a threefold increase in a single patient age group over a short
time period without a concomitant increase in younger patients with similar
underlying conditions. Furthermore, using the available data, no differences in the
types of underlying illnesses could be detected between patients before and
after the increase (Table 6). Whilst there have been changes in patient treatments
which may have long term modulation of the immune system (e.g. statins and
tumour necrosis factor-alpha inhibitors) it is not possible with current data to
ascertain if these are increasing overall risk for listeriosis.
22
Table 6. Underlying illnesses in listeriosis patients aged 60 years and

over: England and Wales
Underlying illnesses 1993-2000 2001-2004
Cancer 42% 43%
Autoimmune 13% 14%
Cardiovascular 13% 12%
Alcohol related 3% 4%
Renal 3% 5%
Diabetic 3% 3%
Hepatic and biliary 2% 1%
Other 20% 18%
Source: Gillespie et al 2006
Changes in medical practice which may render the elderly at increased risk of
listeriosis
Treatment of haematological malignancy
4.14 There has been a trend for older patients to be treated more
aggressively, with more intensive chemotherapy, often using
chemotherapeutic agents which have only become available in the last 10
years. Indeed, national trial protocols are now tending not to state an upper
age limit and it is left to the discretion of the enrolling clinician to assess
patient's suitability for chemotherapy (Smith. Personal communication 2008).
In the GELA (Groupe d'Etude des Lymphomes de l'Adulte) study, elderly
patients with diffuse large B-cell lymphoma were randomized to two regimens
CHOP and CHOP-R, the latter containing rituximab, which is a B lymphocyte-
depleting monoclonal antibody (Coiffier et al, 2002). Patients treated with the
latter manifest better outcomes than the former (Coiffier et al 2007) and
CHOP-R is widely used in the UK in elderly individuals. Rituximab has been
associated with listeriosis (Ng and Lim, 2001).
4.15 The combination of cyclophosphamide plus fludarabine (Rai et al, 2000),

is increasingly used in the management of chronic lymphocytic leukaemia,
which is predominantly a disease of the elderly and, following publication of
the results of the MRC CLL4 trial, is now recommended as standard therapy for
this condition (Catovsky et al, 2007). The association between listeriosis and
fludarabine (a purine analogue) is well recognized (Hequet et al, 1997; Cleveland
and Gelfand 1993; Anaissie et al, 1992).
4.16 The protein kinase inhibitor, imatinib, has now been recommended for
some forms of chronic myeloid leukaemia (CML; NICE(a), 2003). The median
age of diagnosis of CML is 67 years. Cases of listeriosis associated with patients
taking this drug have been reported (Ferrand et al, 2005).
23
Management of solid organ malignancies
4.17 As with haematological malignancies, there have been changes in the

management of those of solid organs over the last 10 years. For example, the
new antimetabolites capecitabine and tegafur have been recommended by
the National Institute for Health and Clinical Excellence for the management
of metastatic colorectal cancer, a condition in which 40% of individuals are
over 75 years at diagnosis (NICE(b), 2003). Similarly 50% of patients diagnosed
with lung cancer are aged 70 years of age and over and there has been a trend
to treat older patients more aggressively including the use of second line
treatment for individuals with small cell disease.
Statins
4.18 Although this category of drugs was introduced in the late 1990s, their
use has increased markedly since then, with prescriptions in England alone
more than doubling in the three year period to 2007 (Department of Health(a),
2007). These drugs are not contra-indicated in the elderly and, indeed a recent
meta-analysis demonstrated a clear benefit for statins in the elderly (defined
as 65 years and over) (Afilalo et al, 2008). Statins are acknowledged to have
immunomodulatory effects, especially on cellular immune function and they
may even play some role in the prevention of solid organ transplant rejection
(Steffens and Mach, 2006; Kobashigawa and Patel, 2006). The implications of
this in terms of increasing risk of listeriosis are unclear. Interestingly, although
L. monocytogenes HMG-CoA reductase is only weakly inhibited by these
drugs (Theivagt et al, 2006), atorvastatin and lovastatin at physiological
concentrations reduced intracellular proliferation of Salmonella Typhimurium
both in vitro and in an animal model (Catron et al, 2004). Statins change
cholesterol and membrane properties, which may decrease susceptibility to
infection, but may also increase sensitivity to infection in other ways.
Disease modifying anti-rheumatic drugs (DMARDS)
4.19 Although rheumatologists are less likely to employ aggressive DMARD

therapy in elderly patients with rheumatoid arthritis (Fraenkel et al, 2006;
Tutuncu et al, 2006), drugs such as etanercept, infliximab and leflunomide are
widely used to treat such patients. These agents have a well recognized
association with listeriosis e.g. (Kesteman et al, 2007; Schett et al, 2005).
Antisecretory Agents
4.20 Functional achlorhydria as a result of antisecretory drug therapy for

dyspepsia-related conditions such as gastro-duodenal ulceration and gastro-
oesophageal reflux disease is also an important risk factor for GI infection.
Inhibition of stomach acid increases susceptibility to listeriosis in animal
models (Schlech et al, 1993). An association between PPI and
campylobacteriosis (Neal et al, 1996) and other gastro-intestinal (GI) infections
24
(Leonard et al, 2007) has been noted and there is increasing evidence to
suggest that PPIs may be a risk factor for the development of Clostridium
difficile-associated disease although this still remains controversial (Lowe et
al, 2006). Over recent years, proton pump inhibitors (PPI) have displaced H2
receptor antagonists because of the near total achlorhydria induced by the
former. Prescription Pricing Authority data show a steady rise in the cost of
prescribing for dyspepsia since the introduction of PPIs. In 1999, 471 million
was spent; 323 million on PPIs, 124 million on H2RAs and 24 million on
antacids. The costs and numbers of prescriptions for dyspepsia have risen
steadily between 1991-1999, (Fig. 5). PPI prescribing has increased steadily, with
little substitution of either antacids or H2 receptor antagonists (H2RAs). Indeed,
following the introduction of the first generic PPI (omeprazole) in 2002
prescriptions doubled in the ensuing 5 years. PPIs are now one of the most
frequently prescribed classes of drug (although <60-70% of prescriptions in
either community or hospital settings are deemed inappropriate) (Forgacs and
Loganayagam, 2008).
Fig. 5. Net cost of dyspepsia medication, England 1991-99
500,000.0 Antacids
Cisapride
450,000.0 H2-receptor antagonists
Proton pump inhibitors
400,000.0 All of BNFsection 1.3
350,000.0
300,000.0
1000
250,000.0
200,000.0
150,000.0
100,000.0
50,000.0
0.0
1990 1991 1992 1993 1994 1995 1996 1997 1998 1999 2000
Year
Source: http://hcna.radcliffe-oxford.com/dyspepsia.htm
Non-behavioural factors which may increase susceptibility to gastro-

intestinal infection (and pathogens whose sole/primary portal of entry is the
gastro-intestinal tract)
4.21 GI infection occurs more frequently in the elderly than in younger

adults. Factors cited as contributing to the increased risk of infection are
gastric atrophy, decreased intestinal mobility, altered regional microflora and
gut mucus secretions (Klontz et al, 1997).
25
Immunosenescence
4.22 There are many mechanisms which contribute to the process of

immunosenescence (Castle et al, 2007), but probably the most important of these
is a decline in T lymphocyte function (Hakim and Gress, 2007; Aw et al, 2007)
(e.g. decreased Th1 response, thymic involution) which would predispose
individuals to an increased risk of infections caused by facultative intracellular
bacteria, such as L. monocytogenes. Declining T cell function in the elderly has
been cited as an explanation for findings from a study which reported that the
factors which increased the risk of contracting listeriosis were also associated with
death in patients under 70 years, yet for patients over 70 years, the presence of a
predisposing factor did not add to the risk of death (Gerner-Smidt et al, 2005).
Malnutrition
4.23 Malnutrition has increased in the elderly (British Association for Parenteral
and Enteral Nutrition, 2003). For example, patients aged 80 years and over are
five times more likely to be malnourished than those 50 years and under, and the
importance of adequate nutrition for elderly patients in hospitals and care
homes has recently been recognized with the publication of Improving
Nutritional Care (Department of Health (b), 2007). Malnutrition has been
reported as a risk factor for listeriosis (Gallagher and Watanakunakorn, 1988).
Other measures of increased susceptibility to listeriosis in the elderly
4.24 Underlying co-morbidities might predispose to listeriosis in the elderly

and it would be of value to determine whether for a given age group there is
more co-morbidity than in a comparator cohort of, say, 10 years ago. There are
many tools to quantify co-morbidity such as the Charlson, Elixhauser and
Kaplan Feinstein Indices, some of which are tailored for use in the elderly
e.g. the Geriatric Index of Co-morbidity (CIG). However, an extensive literature
search failed to identify studies which have addressed this hypothesis.
Conclusions
4.25 Medical advances have resulted in the UK human population surviving
for longer. Elderly individuals are more likely to have underlying co-morbidities,
which are acknowledged to predispose to listeriosis than those in younger age
groups. Elderly patients are increasingly likely to receive immunosuppressive
therapies for chronic conditions which are known to increase the risk of
listeriosis. However, current data collection methods are insufficiently refined
to determine the extent to which, if any, changes in the use of
immunosuppresive or antisecretory therapies in elderly patients have resulted
in an overall increased risk of listeriosis in this age group.
the population.
26
Recommendations
4.27 Studies should be undertaken to investigate whether trends in the
management of conditions which are treated with immunosuppressive or
antisecretory agents might have contributed to the overall increase in the risk
for listeriosis.
4.28 A retrospective case-controlled study could also identify with greater

accuracy those underlying conditions which are most associated with
listeriosis in the elderly.
4.29 Data collected prospectively as part of the investigation of cases of

listeriosis should include more detailed information relating to underlying
comorbidities and their drug management.
Hypothesis 3: The pathogen, L. monocytogenes has

become more virulent and new strains are more capable
of causing infection which manifests as bacteraemia
4.30 Changes in the virulence of L. monocytogenes might explain the change
in disease presentation. However, the increase has involved multiple subtypes,
making this unlikely. However, the growth and behaviour (in vitro, in vivo, in
foods and in the environment) of current L. monocytogenes strains as
compared with those isolated prior to the upsurge has not been examined.
Furthermore, comparisons with strains from other European countries also
experiencing an increase in incidence have not been performed.
4.31 Jacquet et al. (2004) reported that isolates from food were more likely
to express a truncated version of the internalin A protein than those causing
disease in humans. However, virulence is a product of the expression of
multiple genes (Liu et al, 2007) and phenotypic and genotypic tests are not
routinely available to characterise the expression of all virulence genes.
Furthermore, since the upsurge was confined to a restricted patient age group,
this is more likely to reflect increased risk due to higher exposure through
consumption of specific food types and by differences in behavioural
practices of food storage and preparation.
4.32. Complete genome sequences are available for several different

L. monocytogenes strains and there is now a considerable body of information
available on genes associated with the virulence of L. monocytogenes, most of
which encode cell surface structures or secreted products. However, there is
limited information on polymorphisms which occur naturally within these
virulence genes which might affect the ability of this bacterium to cause
infection. Although genes have been identified as essential for virulence of this
bacterium, the exact roles in invasion of the entire host is less well understood.
Patients involved with the recent upsurge with bacteraemia have been shown
to be more likely to have disturbances of the gastrointestinal tract. Virulence
27
genes may have a role for survival and invasion of this organ. These genes might
include putative virulence factors for survival in the stomach, e.g. glutamate
decarboxylase and antiporter proteins gad, betL, gbu and opuC. These proteins
result in a notable increase in cytoplasmic pH of the bacterium (Gahan and Hill
1999), thus potentially enhancing survival in the stomach. Having survived the
stomach, there is some evidence that genes associated with bile salt tolerance
and hydrolysis (btlb and bsh) are involved with survival in the small intestines
as well as invasion via the bile duct (Dussurget et al, 2002). Finally, there is
invasion of intestinal cells mediated by the internalin A and B surface proteins.
Internalin A has been shown to be more important for invasion of intestinal
epithelial cells and variations have been reported in this gene (Olier et al, 2003;
Rousseaux et al, 2004; Jacquet et al, 2004). However, these are part of a family
of surface located proteins and the roles of other internalins (inlC, inlJ, inlE, inlF,
inlG and inlH) may also have a role in virulence (Sabet et al, 2005).
4.33. Characterisation (typing) methods are well developed and a variety of

molecular methods (e.g. molecular serotyping, amplified fragment
polymorphism and pulsed field gel electrophoresis) are routinely used for strain
differentiation. However diversity within L. monocytogenes detected by these
typing methods does not generate information on possible differences in the
virulence of organisms. It has not been possible to exclude the possibility that
the increase in incidence was due to changes in the bacterium. However,
multiple strains were identified with the increase in listeriosis in patients over
60 years of age, hence these factors are likely to be of importance.
Conclusion
4.34 It is possible that specific pathogen factors occurring across multiple
L. monocytogenes strains allow increased infection in older age groups.
Changes in the food chain, such as alterations in food preservation
technologies, may have served to select such strains. However, this is open to
speculation and there is no in vitro evidence to support this hypothesis.
Recommendation
4.35 Work is needed to develop in vitro methods of investigating the
frequency of specific genes or gene polymorphisms associated with
differences in the pathogenicity of L. monocytogenes.
Hypothesis 4: Levels of exposure have increased

4.36 Common source foodborne outbreaks have been reported due to a single
strain of L. monocytogenes which has a higher attack rate for specific members of
the population (e.g. pregnant women, Linnan et al, 1988; non-pregnant
immunocompetent adults Bla et al, 1995; or non-pregnant immunocompromised
adults Fleming et al, 1988), despite the fact that food vehicles were on general sale
28
and were consumed by a much larger section of the population. The common
source clusters which were identified (Table 5) constituted a small proportion of all
cases and did not, therefore, account wholly for the increase in incidence. The
upsurge overall had a similar seasonality to listeriosis in previous periods, occurred
in conjunction with multiple underlying illnesses, in both sexes, across multiple
regions and was caused by multiple L. monocytogenes strains. It is therefore
unlikely that the upsurge reflects a conventional common source food-borne
outbreak confined to older members of the population.
4.37 Unusual clusters of listeriosis due to multiple L. monocytogenes strains

occurring within distinct regions have been reported in Europe and the USA
(Rocourt et al, 1982; Schwartz et al, 1989), which have some similarities to the
current epidemiological pattern but on a national level and over a prolonged
period. Possible explanations previously suggested have included additional
cofactors (possibly infections), which increase susceptibility to infection, multiple
food contamination events due to a common cause, or general changes in
manufacturing and retailing practices for food. It was previously suggested that a
co-infecting organism (probably in the enteric tract) might increase susceptibility to
serious systemic listeriosis (Schwartz et al, 1989). This is certainly possible, although
we are not aware of significant increases in enteric infections concomitant with the
upsurge described here. Since listeriosis is predominantly food-borne, the upsurge
may reflect multiple food contamination events, which, combined with changes in
manufacturing processes or specific eating habits, results in increased exposure to
this bacterium, and this will be discussed in the following section.
Listeria in foods
4.38 Foods traditionally considered high risk with regards to

L. monocytogenes and thus listeriosis all generally have the following similar
characteristics (Bell and Kyriakides, 2005)
Manufactured with no processing step capable of destroying

Listeria spp. eg. cooking or
Exposed to post process contamination e.g. slicing
Product with little or no preservation factors e.g. neutral pH, low
salt, high moisture, etc.
Sold with long shelf life under chilled conditions
Consumed as a ready-to-eat product
4.39 Foods falling into these groups are therefore predominantly chilled,
ready-to-eat foods such as:
Cooked meats and pt

Ready meals (not designed to be fully cooked)
29
Soft ripened cheeses

Cooked fish and shellfish
Dips (non pH-controlled)
Sandwiches
4.40 The properties of L. monocytogenes favour transmission through food and

a wide variety of food and food matrices will support the growth of this
bacterium, which, especially in food with a long shelf life (>10 days), can become
very heavily contaminated. Such problem food types which support the growth
of L. monocytogenes include soft cheese, milk, pt, frankfurters and other
sausages, cooked meat and poultry, smoked fish and shellfish, processed
vegetables and some cut fruit including melon. Foods unable to support the
growth of L. monocytogenes are defined in EC No. 2073/2005 as those with: pH
4.4; or aw 0.92; or pH 5.0 and aw 0.94. Microbiological models are available to
predict the growth of this bacterium under defined conditions. Growth can be
localised within specific areas of an individual food, either because of the source
of contamination (i.e. within cut or contact surfaces or where raw products have
been added) or because of the physicochemical properties of the foods such as in
the areas of higher pH associated with the rind or with mould growth within a soft
cheese. The tolerance of the bacterium to sodium chloride and sodium nitrite, and
the ability to multiply, albeit slowly, at refrigeration temperatures (the doubling
time at 4C is 1 - 2 days) makes L. monocytogenes of particular concern as a post-
processing contaminant in long shelf life refrigerated foods. The widespread
distributionof L. monocytogenes and its ability to survive on dry and moist
surfaces within food manufacturing environments for extended periods favours
post-processing contamination of foods from both raw product and factory sites.
4.41 Listeria spp. grow well on a wide variety of non-selective laboratory media.
However, for isolation from food and environmental sites, selective media are
required. A variety of selective and differential media allowing the isolation of
L. monocytogenes are now generally available, and the ability to isolate and
recognise this bacterium is well within the capabilities of the majority of food,
water and environmental testing laboratories. L. monocytogenes has been
isolated from numerous types of raw, processed, cooked and ready-to-eat foods,
as well as food production sites and the environment (Table 7).
4.42 Selective isolation methodologies are available with agreed and

standardised protocols, which allow both presence/absence tests, as well as
enumeration of the pathogen. The methods are robust, not least because of the
limited phenotypic variation within this genus, and provide qualitative and
quantitative data within the usual confines of sampling error and distribution of
micro-organisms within food matrices.
30
Table 7: UK Food surveys of Listeria contamination in foods, 1997-2007
Meat and fish
Survey title Funded/ Start End Food type No. of L. monocytogenes

carried out by date date samples
tested Total no. Prevalence Level
positive rate (%)
A UK wide microbiological FSA March Sept Sliced cooked 1,691 Report Report Report pending
survey of retail sliced cooked 2007 2007 meats pending pending
meats and pts with particular
reference to Listeria Pts 1,651 Report Report Report pending
monocytogenes pending pending
Survey of the microbiological North West Sept Aug Sliced cooked 1,127 82 7.3 15 samples
examination of freshly sliced LAs and FEMS 2006 2007 meats at point 10-100 cfu/g
cooked meat from the point of NW testing of sale 5 samples >100
sale and after 48 hours laboratories cfu/g
refrigeration at 6C with a focus
on Listeria spp. (North West of Sliced cooked 1,127 Data not Data not 21 samples
England)5 meats after 48 provided provided 10-100 cfu/g
hours 31 samples
>100 cfu/g
A UK wide microbiological FSA July Nov Hot smoked 1,878 66 3.4 63 samples
survey of retail smoked fish 2006 2006 fish <100 cfu/100g
with particular reference to the 3 samples
31
presence of Listeria >100 cfu/g
monocytogenes6
Cold smoked 1,344 236 17.4 236 samples
fish <100 cfu/g
5 Unpublished data from study undertaken by the Cheshire, Cumbria, Greater Manchester, Lancashire and Merseyside Food Liaison Group and the Health Protection Agency's Food and
Environmental Microbiology Services North West. For more info see press release at http://www.hpa.org.uk/webw/HPAweb&HPAwebStandard/HPAweb_C/1211528160312?p=1204186170287
6 http://www.food.gov.uk/science/surveillance/fsisbranch2008/fsis0508
Meat and fish continued

tested Total no. Prevalence Level (cfu/g)
positive rate (%)
32
A UK wide survey of FSA March June Raw beef joints, 3,249 Available Available in Available in 2009
microbiological contamination 2006 2007 steaks and in 2009 2009
of raw red meats on retail sale chops
Raw pork joints, 1,693 Available Available in Available in 2009

steaks and in 2009 2009
chops
Raw lamb 1,056 Available Available in Available in 2009

joints, steaks in 2009 2009
and chops
End of shelf life study of LACORS/HPA Sept Mid Modified 2981 143 4.8 96 samples
modified atmosphere packed 2003 Nov atmosphere <20 cfu/g
and vacuum packed ready-to- 2003 packed and 20 samples
eat meats from retail premises7 vacuum packed 20-100 cfu/g
ready-to-eat 27 samples
meats at end >100 cfu/g
of shelf life (range 102 106)
Microbiological examination of LACOTS/ June July Cold sliced 3494 Data not Data not 8 samples
cold ready-to-eat meats from PHLS 1998 1998 ready-to-eat available available 10-100 cfu/g
catering establishments7 meats 5 samples

>100 cfu/g
7 Further information and full survey reports are available on the LACORS website at: http://www.lacors.gov.uk/lacors/ContentDetails.aspx?id=3512&authCode=4988458
Fresh produce

positive rate (%)
Survey of Listeria on pre- LACORS/HPA May June Pre-packed 2,686 130 4.8 2 samples
packed mixed salads at retail8 2005 2005 mixed salads >100 cfu/g
Survey of pre-cut fruit, European July Dec Pre-cut fruit 997 78 7.8 Data not available
sprouted seeds, unpasteurised Commission 2002 2002
fruit and vegetable juice from (sampling by Sprouted seeds 808 28 3.5 Data not available
production and retail premises LACORS/
in the UK PHLS) Unpasteurised 291 2 0.7 Data not available
fruit and
vegetable juices
The microbiological LACORS/ Sept Oct Open ready-to- 2934 88 3.0 87 samples
examination of open ready-to- PHLS 2001 2001 eat salad <20 cfu/g
eat prepared salad vegetables vegetables 1 sample 840 cfu/g
from catering and retail
premises7
The microbiological LACORS/ May June Pre-packed 3849 90 2.3 88 samples

examination of bagged PHLS 2001 2001 ready-to-eat <10 cfu/g
33
prepared ready-to eat salad salad 1 sample
vegetables from retail vegetables 10-100 cfu/g
establishments 7 1 sample
>100 cfu/g
The microbiological LACOTS/ May June Ready-to-eat 3200 ND ND ND
examination of ready-to-eat PHLS 2000 2000 organic

organic vegetables from retail vegetables
establishments7
8 Further information and survey report is available on the LACORS website at: http://www.lacors.gov.uk/lacors/ContentDetails.aspx?id=14949
Dairy

positive rate (%)
34
Study on the microbiological European Sept Oct Semi-hard 1,842 18 1.0 16 samples
examination of cheeses made Commission 2004 2004 cheese, un- >100 cfu/g
from raw or thermised milk (sampling by ripened (fresh)
from production LACORS/HPA) and ripened
establishments and retail soft cheese
premises in the UK9
The microbiological LACORS/HPA May June Butter from 3,229 13 0.4 13 samples
examination of butter from 2004 2004 production, <10 cfu/g
production, retail and catering retail and
premises for Listeria catering
monocytogenes and other premises
Listeria spp.7
Survey on Listeria MAFF 1998 1999 Raw cows milk 774 32 4.1 Data not available
monocytogenes in raw cows at retail farms
milk10 in England and
Wales
9 Further information and survey report is available on the LACORS website at http://www.lacors.gov.uk/lacors/ContentDetails.aspx?id=16479
10 Defra UK Zoonoses Reports (1999 - 2006)
Sandwiches

positive rate (%)
NPHS Wales Listeria in hospital LAs and NPHS Oct March Hospital 950 Data not 0.2 Data not available
sandwiches survey11 Wales 2005 2006 sandwiches available
Retail 588 Data not 0.9 Data not available

sandwiches available
Microbiological examination of LACORS/HPA April March Sandwiches 3,249 88 2.7 87 samples

sandwiches from hospitals and 2005 2006 <10 cfu/g
residential/care homes with a 1 sample
focus on Listeria <20 cfu/g
monocytogenes and other
Listeria spp.12
11 Meldrum RJ, Smith RM. Occurance of Listeria monocytogenes in sandwiches available to hospital patients in
Wales, United Kingdom. 2007. J. Food Prot. 70(8):1958-60
12 Further information is available at http://www.hpa.org.uk/hpr/archives/2007/news2007/news3307.htm
35
Other

positive rate (%)
Focused shopping basket LACORS/HPA May April Sliced meats 1484 55 3.7 42 samples
sampling linked to Listeria 2006 2007 (within shelf <10 cfu/g
monocytogenes work life) 3 samples
programme 2006/077 10-100 cfu/g
36
10 samples
>100 cfu/g
Sliced meats 684 29 4.2 18 samples

(end of shelf <10 cfu/g
life) 4 samples
10-100 cfu/g
7 samples
>100 cfu/g
Sandwiches 1088 76 7.0 63 samples

<10 cfu/g
9 samples
10-100 cfu/g
4 samples
>100 cfu/g
Hard cheese 1242 2 0.2 2 samples

<10 cfu/g
Confectionery 515 4 0.8 4 samples

products <10 cfu/g
containing
cream
Spreadable 725 ND ND ND
cheese
Butter 878 ND ND ND
Probiotic drinks 368 ND ND ND

Other continued

positive rate (%)
A study of cleaning standards LACOTS/PHLS Sept Nov Cleaning cloths 1070 57 5.0 Not enumerated
and practices in food premises7 2000 2000
Microbiological examination of LACOTS/PHLS Aug Oct Soft ice-cream 597 2 0.3 2 samples
baked egg custard tarts, soft 1997 1997 mix (L. mono- <100 cfu/g
ice-creams and cold mixes7 cytogenes not
detected in
corresponding
soft ice-creams)
Soft ice-creams 1214 10 0.8 10 samples

(L. mono- <100 cfu/g
cytogenes not
detected in
corresponding
mixes)
37
4.43 Evidence provided to the group from a recent study conducted in the
North West of England examining the contamination of cooked meats, sliced in
retail stores demonstrated that L. monocytogenes was present in 7.3% (82/1127)
of products tested on the day of purchase. Of these, five had levels 100cfu/g.
Of the 82 samples that had the bacterium present on the day of purchase, a
further 26 gave counts of L. monocytogenes 100cfu/g after storage at 6oC for
48h (range 100-2000cfu/g). The same survey reported that only 23% of products
were labelled with the use by information although this varied significantly
between establishments (Supermarkets 74%; Market stalls 6%, Delicatessens 8%,
butchers 7%).13
4.44 Given the relatively low number of cases of listeriosis that occur every
year, even taking into account recent increases, it is possible that poor control at
a small number of food businesses manufacturing high risk products could be a
significant contributing factor.
4.45 The Group was unable to assess whether an increase in shelf life across
chilled commodity areas or the development of new foods would account for
an increased risk of listeriosis as limited information was available. However, the
Group received Ad Hoc information from one large supermarket chain has
shown no major recent increase in shelf life for cooked meats, sandwiches, soft
cheeses, ready meals or pts over the period corresponding to the increase in
cases of listeriosis although shelf life has increased by approximately 10-20% in
many chilled foods over the last two decades. Information from the broader
retail sector is not available.
4.46 It is clear, however, that consumer trends have resulted in foods being
modified to reduce preservative factors in a bid to reduce the detrimental
effects of key food components on public health. Reducing salt is probably the
most significant feature of this trend, promoted by government and the FSA in
terms of targets for industry to reduce salt in key foods and also at the public to
reduce the consumption of salt.
4.47 It has been suggested that reduced controlling factors, together with
improved hygienic production could create environments in food that offer
less competition to organisms such as L. monocytogenes, as competitive
microflora are not present in such high numbers. As such the bacterium can
grow faster and thus present greater risk. This is clearly a possibility although
such improved hygienic conditions should consequently reduce the likelihood
of L. monocytogenes being present. In addition, it is generally the case that
foods do continue to suffer from food spoilage and hence spoilage microflora
continue to feature as components of food.
13 http://www.hpa.org.uk/webw/HPAweb&HPAwebStandard/HPAweb_C/1211528160312?p=1204186170287
38
Social factors food handling and consumption patterns

4.48 Analysis of consumption patterns for the year to August 2007 for over 65s
was presented to the Ad Hoc Group by a major retailer from data supplied by a
major market research company TNS (Annex III). Over 65s shopping and eating
habits were compared to total consumers and the following general trends were
identified:
- Over 65s have more frequent, smaller shopping trips than average
households. (Annex III, Figure 1)
- They are more likely to eat homemade, fresh and chilled foods and less
likely to consume frozen or ambient stable foods (Annex III, Figure 2).
- They over-index (when compared to total consumers) at breakfast, in-

home lunch and teatime occasions i.e. on average over 65s eat
breakfast, in-home lunches and teatime food more than the general
consumer (Annex III, Figure 3).
- In comparison with all other age groups, over 65s are the consumer
group whose primary reason for the meal occasion is health and they
are more concerned about managing health (Annex III, Figure 4).
- In terms of food groups that over 65s over-index, the top ten are
(Annex III, Figure 5);
Marmalade (229); Semi-sweet biscuits (220); Fish/meat pastes (200);

Packet soups (200); Fresh meat pies (200); Tinned fruit (200);
Plain/savoury biscuits (193); Fresh soft fruits (168); Fresh/smoked fish
(164); Custards (164).
- In terms of volume consumption, the top ten foods consumed by

over 65s are as follows (Annex III, Figure 6);
Bread and rolls; Butter and margarine; Breakfast cereals; Fresh fruits;
Total desserts; Total snacks; Fresh potatoes; Cold desserts; Cakes,
tarts and pastries; Total sandwiches.
- In terms of food preparation, over 65s are more likely to consume their
food cold rather than hot and consume considerably more cold foods
at breakfast, lunch, teatime and for in-home snacks when compared
with the total consumers (Annex III, Figure 7).
4.49 Data supplied by the BRC for over 60s food expenditure indicated that
they over-indexed (in comparison with all buyers) in the following categories;
Fresh other meat14 and offal; Fresh meat and pastry; Fresh bacon steaks;
Margarine; Chilled black and white pudding; Fresh/Chilled pastry; Lards and
compounds; Butter; Fresh lamb and Fresh cream.
14 other meat includes veal, game and venison
39
4.50 It was not possible to examine these data in terms of particular

vulnerable groups but clearly this may be important as the patterns of
behaviour for the elderly may not necessarily be representative of that for
those with pre-existing conditions as the cases of listeriosis are occurring
predominantly in the elderly with other risk factors.
4.51 An important consideration in relation to the increase in cases of

listeriosis in the over 60s is the potential that food handling practices in this age
group may be a contributory factor. Extended storage of chilled foods beyond
the use by date or poor temperature could allow low levels of the bacterium
to increase in foods to hazardous levels prior to consumption.
4.52 Information on the food safety perception and practices in older age
groups was reviewed. A pilot study conducted in the UK in the early 2000s
involving 9 elderly individuals (n=9 focus group; n=16 home observation &
interview) indicated that most had not measured their refrigerator temperature
and did not know what it should be. The majority gauged the correct
temperature by the feel of the product. Use by dates were understood but not
always followed due to the difficulty in reading labels. Items were purchased
near the end of life as they were sometimes cheaper and they were often kept
for up to a month before consumption (Hudson and Hartwell, 2002).
4.53 A larger study conducted in 1998 (Johnson et al, 1998) of over 65s
concluded that refrigerator temperatures in 70% (451/645) were 6oC, with a
high proportion also reporting difficulty in reading food labels, despite good
knowledge of use by dates.
Conclusions
4.54 It is generally recognised that greatest risk of listeriosis occurs from
consumption of foods where very high levels of L. monocytogenes occur and
thus the aim must be to ensure foods do not have such high levels.
4.55 It was not possible to determine any particular factor in the shopping and
consumption patterns for over 65s that is likely to increase their risk for contracting
listeriosis, although the tendency to eat more homemade, chilled and fresh foods
and to consume more food cold may be important factors. It was not possible to
specifically identify the consumption patterns of vulnerable groups in this age
group but clearly this may be important to identifying any additional risks.
4.56 Information on the food safety perception and practices in older age groups
was limited but did identify factors that could contribute to growth of
L. monocytogenes in already contaminated foods such as keeping foods beyond
their use-by dates or not keeping them refrigerated at suitable temperatures.
4.57 While there is no recent national data source about the shopping, food
storage, cooking and eating behaviours of all over 60s, the Low income diet and
40
nutrition survey (Nelson et al, 2007), has data on this for the over 60s in the most
materially deprived households in the UK. People over 65, ethnic minorities and
people with self reported illness were over-represented in this national sample
of the bottom 15% in income of the UK population. Further analyses of this
study would throw some light on the food purchase and handling behaviour of
this group at risk of L. monocytogenes and provide a basis for identifying how
to research this more generally among the over 60s.
4.58 In addition, it might be possible to gain further insight into how the over
60s manage food purchase, storage and cooking through analysis of existing time
use studies. Diary-based studies are the more appropriate method of obtaining
this information (Gershuny J. Personal communication, 2008). Analysis of the
existing diary based study Home OnLine conducted between 1998 and 2001
would provide a useful starting point and if this proved fruitful, further research
might be undertaken to look at more recent behaviour.
Recommendations
4.59 Maintaining targeted active surveillance for Listeria spp. in foods is
important to understanding if the control of the bacterium is improving or
deteriorating and regular surveys examining a wide range of commonly
purchased foods (shopping basket surveys) that the bacterium can be a
contaminant of may be useful. However, the potential for the bacterium to
contaminate and grow in retail and catering bought foods is important and any
survey should also consider such foods.
4.60 Information on the food consumption patterns of over 60s with

particular reference to vulnerable groups in this age group is necessary in order
to better inform risk management options.
4.61 A study on the food handling behaviours of over 60s including those in
vulnerable groups is recommended in order to better understand factors
potentially contributing to increasing the risk of listeriosis.
4.62 Studies in the home would be of particular benefit to include food

storage behaviour, refrigerator temperatures, adherence to use by date and
analysis of foods for L. monocytogenes.
4.63 Data on control subjects and from listeriosis patients of similar age
should be collected to identify risk factors and allow an evidence basis for
food safety advice to vulnerable groups. Understanding the impact of this on
the growth of the bacterium in food using modelling/challenge studies is
recommended to assess the risks.
4.64 It is also recommended that the FSA refers this Report to its Social
Science Research Committee to consider the food storage and handling
practices of elderly people in the home.
41
Chapter 5: Risk management
Legislative limits
European limits
5.1 In the UK and the rest of Europe, Regulation (EC) 2073/2005 (as
amended) establishes microbiological criteria for L. monocytogenes in ready-
to-eat (RTE) foods. Three food safety criteria have been defined, establishing
different limits according to the target group of consumers or the potential for
the food to support growth of the bacterium. Any product which does not
comply with these limits must be withdrawn from the market.
5.2 Criterion 1.1 applies to all RTE foods intended for infants or for special
medical purposes. A limit of absence in 25g throughout the product shelf life
applies.
5.3 Criterion 1.2 applies to all other RTE foods which support the growth of
L. monocytogenes. Different limits apply depending on whether the
manufacturer can demonstrate that growth has been taken into account in
setting the product shelf-life, as follows:
a) A limit of 100 cfu/g applies throughout the product shelf-life where

growth has been taken into account and manufacturers can
demonstrate compliance with this limit.
b) A limit of absence in 25g applies at the end of the manufacturing

process before the product is placed on the market where growth
has not been taken into account (or manufacturers are unable to
demonstrate compliance with the limit of 100 cfu/g throughout the
shelf-life).
5.4 The Commission produced a Discussion Paper in February 2008 aiming to

clarify the requirements of criterion 1.2 and promote harmonised
implementation. Since this time, EC guidance on L. monocytogenes shelf-life
studies has been developed, which may be sufficient to address the need for
better harmonisation. In addition, the 1-5 December 2008 meeting of the
Codex Committee on Food Hygiene agreed to advance Annex II on
Microbiological Criteria for Listeria monocytogenes in Ready-to-Eat Foods to
step 5/8 which provides for co-existence of US and EU approaches (i.e. absence
in 25g and 100cfu/g) considered to give equal protection to public health. The
Commission is currently reconsidering the need for changes to criterion 1.2 in
light of these developments. The UKs strict interpretation for products under
42
1.2b is that there is no criterion for such products when they are placed on the
market (i.e. when the manufacturer is unable to demonstrate compliance with
the limit of 100 cfu/g). In practice, this means if L. monocytogenes is detected
when such products are on the market, a risk assessment will be conducted by
the appropriate authorities to determine whether any action is required to
protect public health. Regulation 2073/2005 is unlikely to provide the legal base
for action in these circumstances.
5.5 Criterion 1.3 applies to all other RTE foods unable to support the growth
of L. monocytogenes. A limit of 100 cfu/g throughout the product shelf-life
applies. Products with pH 4.4 or a water activity of 0.92, products with pH
5.0 and a water activity of 0.94, products with a shelf-life less than five days
are automatically considered to belong to this category.
5.6 Prior to the introduction of Regulation (EC) 2073/2005 the European

Commissions Scientific Committee on Veterinary Measures relating to Public
Health (SCVMPH) opinion on L. monocytogenes, published 23 September 1999,
recommended that the concentration of L. monocytogenes be maintained at
levels below 100 cfu/g in ready-to-eat foods (European Commission 1999). It was
the conclusion of the SCVMPH that levels below 100 cfu/g represent a very low
risk for all population groups. The Public Health Laboratory Service (PHLS)
guidelines, published 3 September 2000, state that levels below
100 cfu/g are acceptable, but that L. monocytogenes at 100 cfu/g or above
should be considered unacceptable or potentially hazardous (Gilbert et al, 2000).
5.7 Regulation (EC) 2073/2005 was introduced in January 2006. The number
of incidents15 involving L. monocytogenes that have been reported to the
Agency has increased since this legislation came into force (i.e. 2003; 12
incidents, 2004; 14 incidents, 2005; 10 incidents, 2006; 27 incidents, 2007; 17
incidents). However, it is possible that additional factors have also contributed
to this increase (e.g. real effects, improved reporting or the use of themed
food surveys). It would be worthwhile revisiting this observation once there is
a better understanding of the basis for the increase in cases seen in the UK and
other EU Member States.
US limits
5.8 Since the 1980s, the USA has operated a zero-tolerance policy for
L. monocytogenes in ready-to-eat foods. Recently, the United States Food
and Drug Administration has proposed a tolerance of up to 100 cfu/g
L. monocytogenes for ready-to-eat foods that cannot support the growth of
L. monocytogenes.
15 Please note that the Agency defines an incident as any event where, based on the information
available, there are concerns about actual or suspected threats to the safety or quality of food that could
require intervention to protect consumers interests. Not all of the incidents referred to in the figures
above involved a breach of the legislation, although in all cases an investigation was conducted to
determine whether there could be a risk to public health.
43
Food industry listeria controls

5.9 Food manufacturing controls to prevent contamination by Listeria spp.
have improved over the last two decades, following the identification of
contaminated food as a significant cause of listeriosis (Table 8). Chilled, ready-
to-eat foods are produced using HACCP principles that aim to identify where
the hazard can occur in the manufacturing process and at what steps measures
can be put in place to eliminate the hazard or reduce it to an acceptable level
(CFA, 2006).
Table 8: Changes in the rates of L. monocytogenes contamination of
foods examined in England and Wales
% with L. monocytogenes
Year Region Total
number of
samples Total 102-103/g >103/g
Soft
cheese
1987 London 222 10% 0.5% 5%
<1989 England and Wales 1130 6% NK >1%*
1988-1989 England and Wales
Cow 1135 6% <0.1% 1%
Goat and ewe 617 4% 0 0.2%
1989-90 North Yorkshire 131 0 0 0
1991-92 Bristol 251 0.4% 0 0
1995 England and Wales 1437 1% 0 0
1991 England and Wales 356 0 0 0
Pt
<1989 England and Wales 696 17% NK >2%*
1989 South Wales 216 35% 3% 7%
1989 England and Wales 1698 10% 1% 2%
1989-90 North Yorkshire 161 10% 2% 0
1990 England and Wales 626 4% 1% 0.3%
1991-92 Bristol 40 0.5% 0 0
1993 England and Wales 29 3% 0 0
1994 England and Wales 3065 3% 0.2% 0.4%
2000 England and Wales 26 0 0 0
2000 North East England 72 1% 0 1%
2000 England, Wales, 1178 2% 0 0
Scotland and
Northern Ireland
NK = not known; *some samples enumeration not performed.

Data from McLauchlin J. Listeria. In Motarjemi Y, Adams M (eds). Emerging foodborne
pathogens. Woodhead Publishing, Cambridge, 2006. pp406-428.
44
5.10 The bacterium is ubiquitous in the environment and therefore unless

the food is subject to a cooking process (achieving a heat process equivalent
to 70C for 2 minutes) in a hermetically sealed container it is difficult to
completely guarantee its absence from all chilled, ready-to-eat foods at all
times. As most chilled foods are not treated in this way, most focus is placed
on preventing contamination of foods from equipment and the environment
and thus minimising the frequency with which the bacterium contaminates a
food or alternatively preventing growth to high levels through shelf life
restriction or product formulation.
5.11 Many foods that allow the growth of Listeria spp. are included in the
FSA targets for salt reduction and include ready meals, cooked meats and
sausages, cheeses and sandwiches (ACMSF, 2005). ACMSF has reviewed this
advice and has recommended that manufacturers consider the impact on
microbiological safety when making formulation changes to the key
controlling factors such as salt in specific products (ACMSF, 2006).
5.12 Provided that producers of chilled, ready-to-eat food are operating to

current recognised industry standards, disciplines will be in place in large
manufacturing plants to segregate products and people between the raw or
low risk side of the factory from the ready-to-eat or high risk side.
Movement of products and equipment from the low risk to the high risk side
of the factory occurs through a controlled area e.g. cooker or washer and
movement of people occurs through changing areas where clothing including
footwear and outer garments are changed to avoid contamination. Air flow
and drainage is designed to ensure they flow from high risk to low risk,
thereby minimising transfer of contamination via these routes. (It should be
noted that this situation may not be fully replicated in smaller production
units, where the application of proportionate risk based controls may result in
different arrangements.)
5.13 The level of control varies depending on the risk presented by the
finished product in terms of potential for contamination and growth. For
example, controls in place for cooked, sliced meat will be greater than those in
factories producing ready-to-eat washed salads as the former have longer
shelf lives and offer greater opportunity for growth of any contaminating
organisms.
5.14 Such control includes measures to prevent Listeria spp. building up in

the environment and on equipment, aspects recognised as key to preventing
contamination of ready-to-eat foods. Hence, thorough cleaning and
disinfection of the chilled, ready-to-eat food production environments occurs
on a daily basis and more frequently for much of the equipment and product
contact surfaces. Methods to reduce the spread of the organism in the
environment such as use of low water pressures and minimising water usage
during production are widely recognised and applied in the industry.
45
5.15 Analytical testing of both the environment and the product to verify
that controls have been effective in managing the organism has been routinely
applied for many years. It is recognised that microbiological testing can form
an integral part of an effective HACCP plan (SANCO/4198/2001 Rev 21) and in
2006, such testing became a mandatory requirement under Commission
Regulation on Microbiological Criteria for Foodstuffs (2073/2005/EC) (see 5.7).
5.16 The preventative measures in place in the food manufacturing industry

today as described in paragraphs 5.9 5.15 are believed to be considerably
higher than those in place two decades ago and there is no evidence of any
changes recently that would have led to a significant increase in contamination
of manufactured foods with L. monocytogenes. Indeed, data from recent
surveys for L. monocytogenes in food indicate that whilst the bacterium does
still occur in foods, it is not generally found at high levels and is present at
much lower levels than was the case in the late 1980s.
5.17 Notwithstanding this, it is important to recognise there is a difference

between manufacturing, catering and retail in considering the potential for
food to become contaminated with Listeria spp. Catering and retail outlets,
including delicatessens, handle a high volume of chilled perishable products
that are not necessarily subject to the same controls to prevent contamination
as those produced in major manufacturing units operating high/low risk
principles. Such businesses often receive pre-packaged products e.g. bulk
cooked meats, pt, cheeses etc or they may make them on the premises
themselves e.g. cooked meats. Once open, such perishable products are
subject to cross contamination if equipment is poorly cleaned e.g. slicing
machines, knives, etc, and the environment, people and pests. In addition,
should the product already be contaminated with the bacterium or become
contaminated during handling, preventing growth to high numbers is
dependent on the adoption of strict temperature control and management of
shelf life. Whilst many such products, once opened, are limited in shelf life for
organoleptic reasons, the subsequent handling by the customer may also be
important in ensuring the safety of the product and thus storage instructions
including a durability indicator (Use By) and storage information (Store
refrigerated) are important.
5.18 Identifying poor practices in a small number of businesses is likely to be

very difficult. Many food businesses, especially those supplying large retail
chains and catering companies, are subject to frequent certification audits to
third party food safety standards e.g. BRC global standard for food safety
(certification is currently held by approximately 10,000 food businesses)
together with audits and visits by experienced food technologists from
relevant customers; this is likely to identify poor management of Listeria spp.
Without this, enforcement monitoring would be the only means of identifying
poor practices. Improving the identification of poor practices is likely to be
46
important in identifying poor management of Listeria spp. in food businesses

but it is questionable whether current industry/enforcement scrutiny is
sufficient to identify this if it is happening in a small minority of businesses.
Consumer Advice
5.19 The FSAs consumer advice on listeriosis was originally targeted towards
pregnant women and recommended that this group should avoid all types of
pt (including vegetable) and mould-ripened soft cheeses of the Brie,
Camembert and blue-veined types. In the course of writing this report, the
FSA consulted the Ad Hoc Group on whether this advice should be extended
to vulnerable groups in addition to pregnant women. This action was
considered necessary following several clusters of cases in healthcare settings
and because the increase in listeriosis since 2001 mainly involved the over 60s
with underlying medical conditions. The Ad Hoc Group was content to extend
this advice and suggested that it should also emphasise existing advice on
observing correct temperature control for foods that require refrigeration and
on following use-by dates. The advice on the Agencys website was updated in
July 2008.
5.20 The FSAs website16 currently provides the following advice on listeriosis
to consumers;
Listeria monocytogenes can cause illness in certain groups of people,

such as pregnant women, unborn and newborn babies and people with
reduced immunity, particularly those over 60 (these could include
people who've had transplants, are taking drugs that weaken the
immune system or with cancers affecting the immune system, such as
leukaemia or lymphoma). Among these vulnerable groups, the illness is
often severe and can be life-threatening.
Listeria has been found in certain chilled ready-to-eat foods, such as

pre-packed sandwiches, butter, cooked sliced meats, smoked salmon,
soft mould-ripened cheeses and pts. Eating food containing high
levels of Listeria monocytogenes is usually the cause of illness.
Vulnerable people should avoid eating pasteurised and unpasteurised

cheeses such as Camembert, Brie or chvre (a type of goats' cheese), or
others that have a similar rind, soft blue cheeses, and all types of pt,
including vegetable.
Special care should also be taken to follow the storage instructions on

the food label. Chilled foods should be kept out of the fridge for the
shortest time possible and you shouldn't use food after its 'use by' date.
16 http://www.eatwell.gov.uk/healthissues/foodpoisoning/abugslife/
47
5.21 The Agency also advises pregnant women to ensure that any raw meat,
shellfish or ready meals that they consume have been well cooked until they
are piping hot throughout. This advice relates to other foodborne pathogens
in general and not specifically to L. monocytogenes.
5.22 NHS Direct recognises that listeriosis may affect older people, very
young children and people with lowered immune systems and that Listeriosis
is potentially harmful to unborn babies, so pregnant women need to be very
careful to avoid the infection. NHS Direct currently provides the following
advice on the prevention of listeriosis:17
If you are pregnant:
Don't eat soft mould-ripened or blue-veined cheeses such as

Brie, Camembert, stilton, and goat's cheese. You can still eat hard
cheese, cottage cheese and yoghurts
Don't eat pt
Avoid unpasteurised dairy products (including unpasteurised ice

creams)
You can drink probiotic yoghurt drinks and eat 'live' yoghurt as
long as they have been pasteurised. Check the label
Wash pre-packed salads thoroughly before eating
The risk from cold (pre-cooked) meats and smoked salmon is

fairly low, but you may wish to avoid them while you are
pregnant
Wash your hands before and after handling food
Wash fruit and vegetables
Cook food thoroughly (especially meat, eggs, chilled meals and

ready-to-eat chicken)
Check 'use by' dates
5.23 The HPA recognises that Pregnant women, the elderly and people with
weakened immune systems, including those suffering from cancer, AIDS or
alcoholism, are more susceptible to listeria. HPA currently provides the
following advice on the prevention of listeriosis:
17 Since this report was prepared, NHS Direct has published updated advice on preventing listeriosis.
This can be found at: http://www.nhs.uk/conditions/Listeriosis/Pages/Introduction.aspx
48
How can you avoid getting listeria?
Listeria is unusual because it not only grows at normal room

temperature and up to about 40C, but can grow at low temperatures,
including refrigeration temperatures of below 5C. It is, however, killed
by cooking food thoroughly in conventional or microwave ovens and
by pasteurisation.
Keep foods for as short a time as possible and follow storage

instructions including 'use by' and 'eat by' dates
Cook food thoroughly, especially meat, ensuring that it is cooked

through to the middle
Keep cooked food away from raw food
Wash salads, fruit and raw vegetables thoroughly before eating
Wash hands, knives, and cutting boards after handling uncooked

food
Make sure that the refrigerator is working correctly
When heating food in a microwave follow heating and standing

times recommended by the manufacturer
Throw away left-over reheated food. Cooked food which is not

eaten immediately should be cooled as rapidly as possible and
then stored in the refrigerator
Pregnant women, the elderly, and people with weakened

immune systems should not help with lambing or touch the
afterbirth
5.24 Examples of advice provided to vulnerable groups in relation to

L. monocytogenes by the Authorities in other countries are provided in Table 9.
Conclusions
5.25 The food industry has implemented many controls to prevent the
contamination of foods with L. monocytogenes in the last two decades and
evidence suggests that the incidence and levels of the bacterium at the point
of production and the point of sale are not higher than was detected in the
late 1980s.
5.26 Shelf life management is a key control that can be exercised to reduce
the opportunity for the bacterium to grow to high levels and whilst it is very
difficult to gather data on shelf life increase over recent years, there is no
evidence of marked increase in shelf lives across chilled commodity areas or
49
the development of new commodity foods that would account for increased
risk of listeriosis. Further information on shelf life increases in ready-to-eat
chilled foods over the last 10 years would be useful.
5.27 The bacterium has, however, been found to be present in a number of

chilled ready-to-eat foods, usually at low levels, which probably represent a
low risk, provided subsequent storage time and temperature conditions are
maintained at acceptable levels prior to consumption.
5.28 Preservative factors are important in restricting the growth of the

bacterium when present in foods and trends to reduce factors such as salt may
lead to increased growth of the bacterium if present on such a food.
5.29 Advice to the public to date has focussed on pregnant women. In order
to avoid the risk of listeriosis, the FSA advises pregnant women to avoid all
types of pt (including vegetable), mould-ripened soft cheeses of the Brie,
Camembert and blue-veined types.
5.30 There seems to be very little specific advice targeting the elderly (Cates
et al, 2006), and therefore it is possible that the increase in listeriosis in the
elderly is in part a consequence of not having advice targeted at this age group.
Recommendations
5.31 It is recommended that, based on considerations of foods associated
with transmission of listeriosis and the properties of the bacterium, that
general advice should be developed and communicated to over 60s
(including those in vulnerable groups), as well as those who prepare and
provide their food and provide medical advice about the factors important
to reduce the risk of exposure to L. monocytogenes. Studies should be
carried out to evaluate the impact of such advice on these target groups and
its effectiveness at reducing the incidence of listeriosis.
5.32 The principles of food safety management through the application of

hazard analysis approaches such as HACCP are well established in the food
industry. Universal adoption of these principles by the manufacturing,
catering and retail industry, together with effective enforcement, is a
recognised way of ensuring food safety. Any future advice to the industry and
enforcement authorities given by the FSA should reiterate the particular
importance of temperature and shelf life control, hygiene/cleaning (especially
of equipment susceptible to contamination such as slicing machines) and
formulation of a food in preventing contamination or limiting the growth of
L. monocytogenes in foods.
50
5.33 The provision of durability instructions i.e. Use By dates on perishable

foods sold loose e.g. cooked sliced meats was found to be variable and it is
recommended that the Food Standards Agency reviews the need for
consistent advice on such products. Such instructions should also take
account of age-related deteriorations in eyesight which may be very relevant
to the target population for this advice.
5.34 FSA should work with industry to ensure that factors such as salt levels
of specific products are not changed without considering the impact on the
microbiological safety of the product (ACMSF, 2005).
51
Table 9: Examples of food safety advice on listeriosis provided to vulnerable groups by non-UK Authorities. Please note that this
is not an exhaustive list, but is intended to provide examples of the advice provided by Authorities in other countries. Please also
note that some of this food safety advice may relate to foodborne pathogens in general and is not specific to L. monocytogenes.
Country Vulnerable groups Advice on foods to avoid Website
Australia and Pregnant women Cold meats; unpackaged ready-to-eat from www.foodstandards.gov.
New Zealand delicatessen counters, sandwich bars etc. Packaged, au/_srcfiles/Listeria.pdf
Older people (generally sliced ready-to-eat
52
considered to be persons Cold cooked chicken; purchased (whole, portions, or
over 65-70 years) diced) ready-to-eat
Pate; refrigerated pate or meat spreads
People of all ages whose Salads (Fruit and vegetables); pre-prepared or pre-
immune systems have been packaged salads (e.g. from salad bars, smorgasbords
weakened by disease or etc)
illness Chilled seafood; raw (e.g. oysters, sashimi or sushi),
smoked ready-to-eat, or ready-to-eat peeled prawns
Anyone on medication that (cooked) e.g. in prawn cocktails, sandwich fillings and
can suppress the immune prawn salads
system Cheese; soft, semi soft and surface ripened (pre-
packaged and delicatessen), (e.g. Brie, Camembert,
ricotta, feta and blue.
Ice cream; soft serve
Other dairy products; unpasteurised dairy products
(e.g. raw goats milk)
USA Pregnant women Soft cheeses; Mexican-style soft cheeses (including www.fda.gov
Older adults queso blanco, queso fresco, queso de hoja, queso de
People with cancer, AIDS, and creama and asadero), feta, Brie, and Camembert, blue
other diseases that weaken cheeses and Roquefort. Cheeses made from raw milk.
the immune systems. Refrigerated pts or meat spreads.
Raw (unpasteurised) milk or foods that contain
unpasteurised milk.
Hot dogs, luncheon meats and other ready-to-eat

foods - unless they're reheated until steaming hot.
Meats and seafood - unless it's in a cooked dish
USA Patients with cancer Food safety is very important when your white blood cell www.cancer.org/docroot/E
(WBC) count is low. Infections can be picked up from TO/content/ETO_1_2X_Inf
food and drinks. You can reduce this risk as well by doing ections_in_People_with_C
the following: ancer.asp
Avoid raw milk or milk products and any milk or milk
product that has not been pasteurized, including
cheese and yogurt made from unpasteurized milk
Do not eat raw or undercooked meat, fish, chicken,
eggs, or tofu
Do not eat cold smoked fish
Do not eat hot dogs, deli meats, or processed meats
(unless they have been cooked again just before eating)
Avoid any food that contains mold (for example, blue
cheese, including that in salad dressings)
Avoid uncooked vegetables and fruits
Avoid uncooked grain products
Avoid unwashed salad greens
Do not eat vegetable sprouts (alfalfa, bean, and others)
Avoid fruit and vegetable juices that have not been
pasteurized
Avoid raw honey (honey that has not been
pasteurized)
Do not eat raw nuts or nuts roasted in their shells
Do not drink beer that has not been pasteurized
(home brewed and some microbrewery beers); also
53
avoid brewers yeast
Do not eat any outdated food
Do not eat any cooked food that has been left at
room temperature for 2 hours or more
Avoid any food that has been handled or prepared
with unwashed hands

Talk with your doctor about any dietary concerns you
may have, or ask to talk with a registered dietician.
54
Canada Pregnant women Soft cheeses such as Brie, Camembert, feta and queso www.inspection.gc.ca/
blanco fresco. english/fssa/concen/cause/
People with a weakened Refrigerated pts. listeriae.shtml
immune system Although the risk of listeriosis associated with foods
from deli counters, such as sliced packaged meat and
poultry products, is relatively low, pregnant women
and immunosuppressed persons may choose to avoid
these foods.
Refrigerated smoked fish products unless you have
cooked them, for example, in a casserole.
Germany People with a weakened Do not eat any foods of animal origin raw. www.bfr.bund.de/cd/10966
immune system, older Refrain from eating smoked or marinated fish products,
individuals and pregnant particularly vacuum-packed smoked salmon and
women gravadlax.
Do not eat any raw milk soft cheese and always
remove the cheese rind.
Always prepare green salads themselves and do not
use any cut packaged salads.
Use foods, in particular vacuum-packed foods, as soon
as possible after purchase and well in advance of the
best before date.
Chapter 6: Summary of Conclusions and

Recommendations
Hazard identification and characterisation
Conclusions
6.1 Human listeriosis is a rare but serious disease which occurs most often
in patients with cancer, those undergoing immunosuppressive or cytotoxic
treatment, the elderly (over 60 years of age), the unborn and newly delivered
infants, the pregnant woman, diabetics, alcoholics (including those with liver
disease) and a variety of other conditions.
6.2 Consumption of contaminated food is believed to be the principal route

of infection and common source outbreaks together with sporadic cases occur.
6.3 The majority of cases are/appear to be sporadic and foods associated

with transmission are predominantly ready-to-eat, with extended (usually
refrigerated) shelf-life, capable of supporting the growth of L. monocytogenes.
6.4 Since 2000, the annual number of listeriosis cases reported has
increased and has occurred almost exclusively in patients aged over 60 years
presenting with listerial bacteraemia. This increase is independent of
demographic changes in the population and has resulted in an approximate
tripling in the rate of the disease in those aged 60 years and over in England
and Wales: 3.3-4.7 cases per million were reported between 1990-1992 and 13.2
cases per million in 2007. However, the degree of under-reporting of listeriosis
in the UK has not been recently estimated.
6.5 A similar change in presentation of listeriosis has been reported in

Scotland and Northern Ireland and Germany. Significant increases in cases
were also reported in Belgium, Denmark, France, Lithuania, The Netherlands
and Spain. There is no evidence for a common source relationship between
these changes which have occurred in the UK and those in other countries.
Recommendations
6.6 Pan-European surveillance and epidemiological and microbiological
investigations should be used to investigate changes in listeriosis in different
Member States and to ascertain if there are common generic or risk factors
occurring in the UK with those in other countries.
55
6.7 Studies should be undertaken to develop methods for screening

L. monocytogenes isolates for differences in virulence and investigate the
differences between isolates from different patient groups and time periods.
Consideration of key hypotheses to explain the increase in

listeriosis cases
Hypothesis 1: The rise in cases of listeriosis in immunocompromised people

over 60 years is an artefact associated with improved case recognition
Conclusions
6.8 L. monocytogenes will grow on most non-selective media; therefore
improvements in microbiological media would be unlikely to increase the
diagnosis of listeriosis (McLauchlin 2005). Although the introduction of
mandatory reporting of meticillin-resistant Staphylococcus aureus
bacteraemia in England in 2001 has led to an increase in blood cultures being
taken, this is insufficient to explain the increase or shift in presentation of
listeriosis described here (Anon 2000b, Anon 2005b). Further evidence that the
increase was not due to improved diagnostics is provided by the absence of a
significant increase in the isolation of L. monocytogenes from blood cultures
from patients with CNS infections or from pregnancy-associated cases
(Gillespie et al, 2008). In addition, there has not been an increase in
bacteraemia amongst other foodborne pathogens (i.e. Salmonella and
Campylobacter) in the over 60s. (Gillespie et al, 2008).
6.9 The degree of under-reporting of listeriosis in the UK has not been

estimated recently. An ascertainment ratio of 2 (estimation of the numbers of
cases of illness to the numbers reported to national databases for laboratory
confirmed infections) for human listeriosis was estimated by Adak and
colleagues (Adak et al, 2002). The amount of under-reporting (ascertainment
ratio) for human listeriosis could be estimated by comparing the numbers of
cases reported to national databases with the numbers of cases ascertained in
a subset of diagnostic centres. Since the highest numbers of cases occur in
those 60 years old and over and there is a possibility of surveillance artefact
due to changes in diagnostic procedures having introduced bias, resources
should be concentrated on investigation of incidence in this section of the
population.
6.10 The Second Infectious Intestinal Disease Study will not address this
problem. However, even if significant under-reporting of listeriosis has
previously occurred, the FSA has recently estimated that L. monocytogenes is
responsible for the highest numbers of deaths from a food-borne pathogen
(FSA 2007, Annual report of the Chief Scientist 2006/7). Since the highest
56
numbers of cases occur in those 60 years old and over, resources should be
concentrated to reduce the incidence in this section of the population.
6.11 Our ability to analyse infection trends and understand changes in the
epidemiology would be enhanced by the routine collection of denominator
data for selected medical investigations associated with infection.
Recommendations
6.12 The amount of under-reporting (ascertainment ratio) for human
listeriosis should also be estimated.
6.13 UK surveillance of infection should be enhanced to incorporate data

on the corresponding denominator populations, including numbers of
relevant medical investigations, such as blood cultures, undertaken.
Hypothesis 2: The population predominantly affected by the recent increase

has become more susceptible to infection with L. monocytogenes
Conclusions
6.14 Medical advances have resulted in the UK human population surviving
for longer. Elderly individuals are more likely to have underlying co-
morbidities, which are acknowledged to predispose to listeriosis than those in
younger age groups. Elderly patients are increasingly likely to receive
immunosuppressive therapies for chronic conditions which are known to
increase the risk of listeriosis. However, current data collection methods are
insufficiently refined to determine the extent to which, if any, changes in the
use of immunosuppressive or antisecretory therapies in elderly patients have
resulted in an overall increased risk of listeriosis in this age group.
the population.
Recommendations
6.16 Studies should be undertaken to investigate whether trends in the
management of conditions which are treated with immunosuppressive or
antisecretory agents might have contributed to the overall increase in the risk
for listeriosis.
6.17 A retrospective case-controlled study could also identify with greater

accuracy those underlying conditions which are most associated with
listeriosis in the elderly.
57
6.18 Data collected prospectively as part of the investigation of cases of

listeriosis should include more detailed information relating to underlying
comorbidities and their drug management.
Hypothesis 3: The pathogen, L. monocytogenes has become more virulent

and new strains are more capable of causing infection which manifests as
bacteraemia
Conclusion
6.19 It is possible that specific pathogen factors occurring across multiple
L. monocytogenes strains allow increased infection amongst older age groups,
and these factors may have been selected to increase within the food chain,
for example by changes in the food chain including food preservation
technologies. However, this is open to speculation and there is no in vitro
evidence to support this hypothesis.
Recommendation
6.20 Work is needed to develop in vitro methods of investigating the
frequency of specific genes or gene polymorphisms associated with
difference in the pathogenicity of L. monocytogenes.
Hypothesis 4: Levels of exposure have increased
Conclusions
6.21 It is generally recognised that greatest risk of listeriosis occurs from
consumption of foods where very high levels of L. monocytogenes occur and
thus the aim must be to ensure foods do not have such high levels.
6.22 It was not possible to determine any particular factor in the shopping
and consumption patterns for over 65s that is likely to increase their risk for
contracting listeriosis, although the tendency to eat more homemade, chilled
and fresh foods and to consume more food cold may be important factors. It
was not possible to specifically identify the consumption patterns of
vulnerable groups in this age group but clearly this may be important to
identifying any additional risks.
6.23 Information on the food safety perception and practices in older age
groups was limited but did identify factors that could contribute to growth of
L. monocytogenes in already contaminated foods such as keeping foods
beyond their use-by dates or not keeping them refrigerated at suitable
temperatures.
58
6.24 While there is no recent national data source about the shopping, food
storage, cooking and eating behaviours of all over 60s, the Low income diet
and nutrition survey (Nelson et al, 2007), has data on this for the over 60s in
the most materially deprived households in the UK. People over 65, ethnic
minorities and people with self reported illness were over-represented in this
national sample of the bottom 15% in income of the UK population. Further
analyses of this study would throw some light on the food purchase and
handling behaviour of this group at risk of L. monocytogenes and provide a
basis for identifying how to research this more generally among the over 60s.
6.25 In addition, it might be possible to gain further insight into how the over
60s manage food purchase, storage and cooking through analysis of existing
time use studies. Diary-based studies are the more appropriate method of
obtaining this information (Gershuny J. Personal communication, 2008).
Analysis of the existing diary based study Home OnLine conducted between
1998 and 2001 would provide a useful starting point and if this proved fruitful
further research might be undertaken to look at more recent behaviour.
Recommendations
6.26 Maintaining targeted active surveillance for Listeria spp. in foods is
important to understanding if the control of the bacterium is improving or
deteriorating and regular surveys examining a wide range of commonly
purchased foods (shopping basket surveys) that the bacterium can be a
contaminant of may be useful. However, the potential for the bacterium to
contaminate and grow in retail and catering bought foods is important and
any survey should also consider such foods.
6.27 Information on the food consumption patterns of over 60s with

particular reference to vulnerable groups in this age group is necessary in
order to better inform risk management options.
6.28 A study on the food handling behaviours of over 60s including those in
vulnerable groups is recommended in order to better understand factors
potentially contributing to increasing the risk of listeriosis.
6.29 Studies in the home would be of particular benefit to include food

storage behaviour, refrigerator temperatures, adherence to use by date and
analysis of foods for L. monocytogenes.
6.30 Data on control subjects and from listeriosis patients of similar age
should be collected to identify risk factors and allow an evidence basis for
food safety advice to vulnerable groups. Understanding the impact of this on
the growth of the bacterium in food using modelling/challenge studies is
recommended to assess the risks.
59
6.31 It is also recommended that the FSA refers this Report to its Social
Science Research Committee to consider the food storage and handling
practices of elderly people in the home.
Risk Management
Conclusions
6.32 The food industry has implemented many controls to prevent the
contamination of foods with L. monocytogenes in the last two decades and
evidence suggests that the incidence and levels of the bacterium at the point
of production and the point of sale are not higher than was detected in the
late 1980s.
6.3 Shelf life management is a key control that can be exercised to reduce
the opportunity for the bacterium to grow to high levels and whilst it is very
difficult to gather data on shelf life increase over recent years, there is no
evidence of an increase in shelf lives across chilled commodity areas or the
development of new commodity foods that would account for increased risk
of listeriosis. Further information on shelf life increases in ready-to-eat chilled
foods over the last 10 years would be useful.
6.34 The bacterium has, however, been found to be present in a number of

chilled ready-to-eat foods, usually at low levels, which probably represent a
low risk, provided subsequent storage time and temperature conditions are
maintained at acceptable levels prior to consumption.
6.35 Preservative factors are important in restricting the growth of the

bacterium when present in foods and trends to reduce factors such as salt may
lead to increased growth of the bacterium if present on such a food.
6.36 Advice to the public to date has focussed on pregnant women. In order
to avoid the risk of listeriosis, the FSA advises pregnant women to avoid all
types of pt (including vegetable), mould-ripened soft cheeses of the Brie,
Camembert and blue-veined types.
6.37 There seems to be very little specific advice targeting the elderly (Cates
et al, 2006) and therefore it is possible that the increase in listeriosis in the
elderly is in part a consequence of not having advice targeted at this age group.
60
Recommendations
6.38 It is recommended that, based on considerations of foods associated
with transmission of listeriosis and the properties of the bacterium, that
general advice should be developed and communicated to over 60s
(including those in vulnerable groups), as well as those who prepare and
provide their food and provide medical advice about the factors important
to reduce the risk of exposure to L. monocytogenes. Studies should be
carried out to evaluate the impact of such advice on these target groups and
its effectiveness at reducing the incidence of listeriosis.
6.39 The principles of food safety management through the application of

hazard analysis approaches such as HACCP are well established in the food
industry. Universal adoption of these principles by the manufacturing,
catering and retail industry, together with effective enforcement, is a
recognised way of ensuring food safety. Any future advice to the industry and
enforcement authorities given by the FSA should reiterate the particular
importance of temperature and shelf life control, hygiene/cleaning (especially
of equipment susceptible to contamination such as slicing machines) and
formulation of a food in preventing contamination or limiting the growth of
L. monocytogenes in foods.
6.40 The provision of durability instructions i.e. Use By dates on perishable

foods sold loose e.g. cooked sliced meats was found to be variable and it is
recommended that the Food Standards Agency reviews the need for
consistent advice on such products. Such instructions should also take
account of age-related deteriorations in eyesight which may be very relevant
to the target population for this advice.
6.41 FSA should work with industry to ensure that factors such as salt levels
of specific products are not changed without considering the impact on the
microbiological safety of the product (ACMSF, 2005).
61
Annex I
List of organisations and contributors who

assisted the Group
Dr Iain Gillespie
Health Protection Agency
Ms Sally Barber
British Retail Consortium
Dr Monique Raats
(Food in later life project)
University of Surrey
Ms Esther Cunningham
TNS Worldpanel Usage
UK
Dr Marta Hugas
Scientific Panel on Biological Hazards
European Food Safety Authority
Ms Pia Mkel
Scientific Coordinator
Unit on Zoonoses Data Collection
European Food Safety Authority
Professor Eric Bolton

HPA North West Regional Laboratory
Manchester
Mr Bobby Kainth and Miss Nicola Walker

Microbiological Safety Division
Food Standards Agency
62
Annex II
Terms of reference
To examine the potential risks to vulnerable groups including the elderly in
relation to the microbiological safety of food by:
considering factors that make people vulnerable in order to
define vulnerable groups in relation to foodborne disease
identifying key hazards for key vulnerable groups for review
assessing the impact of changing patterns of food consumption
and behaviour on risks to these groups
assessing/reviewing the value/adequacy of current advice and
controls and whether it is appropriate
advising the ACMSF on the need for changes in
advice/recommendations on vulnerable groups and identifying
gaps/research needs.
Chair
Professor Tom Humphrey (current)
Professor Paul Hunter (April 2007 to December 2007)
Members
Mr John Bassett
Mr Alec Kyriakides
Dr Richard Holliman
Mrs Jenny Morris
Ms Susan Davies (to March 2008)
Professor John Coia
Dr Jim McLauchlin
Ms Ceridwen Roberts
Professor Kevin Kerr
Assessors
Dr Judith Hilton (FSA)
Mr Stephen Wyllie (Defra)
Secretariat
Dr Lucy Foster
Dr Joanne Aish
Mr Adekunle Adeoye
Miss Sarah Butler
63
Annex III
Worldpanel Usage methodology

Worldpanel Usage is the UKs leading, and only continuous
monitor of Food and Drink consumption In and Out of Home.
Sample of 11,000 individuals in 4,200 households
Complete food and drink diary for 2 weeks every 6 months
Record all consumption of food and drink (providing us with

the complete consumption picture from In home/lunchbox to food service
and impulse channels)
Staggered sample so every day of the year is covered
Representative Sample (total GB)
Annual individual and household attitudinal/lifestyle questions

Data delivered quarterly
Current data periods are: 3 months to August delivered in

Nov, 3 months to Nov delivered in February, 3 months to Feb
delivered in May, 3 months to May delivered in August
Figure 1: Over 65s have more frequent, smaller shopping trips
Total Over
Households 65s
55.7bn (+4%) Spend 13.0 bn (+3%)
2,261 (+4) AWP 2,148 (+3%)
216 (+2%) Frequency 289 (+1%)
10.48 (+2%) Trip Spend 7.41 (+2%)
Source: TNS Worldpanel 52w/e 25th March 07
64
Figure 2: Adults 65+ are more likely to eat homemade foods, fresh
foods and chilled foods.
They are less likely to consume frozen and ambient foods.
% of individual meal
occasions
Total In Home, 52 w/e end Aug 2007
Figure 3: Adults 65+ overindex at the breakfast, in home lunch and

teatime occasions. They are also more likely to snack in the home.
They are low lunchbox consumers and are less likely to consume
snacks out of the home.
occasions
Total Consumption, 52 w/e end Aug 2007
65
Figure 4: Adults 65+ are more likely to consume for health and
favourite. This group is the most traditional and also the most health
conscious.
occasions
Figure 5:
Top Foods more likely to be consumed by 65+

Marmalade 229
Semi-Sweet Biscuits 220
Fish/Meat Pastes 200
Packet Soups 200
Fresh Meat Pies 200
Tinned Fruit 200
Plain/Savoury Biscuits 193
Fresh Soft Fruits 168 Traditional and Healthy foods top
Fresh/Smoked Fish 164 the list of foods the 65+ are more likely
Custards 164
Dried Fruits 164
to consume. Sweet favourites such as
Fresh/Chilled Soup 160 biscuits and desserts also feature.
Fresh Medium Fruit 159
Pickles and Chutneys 157
Steamed and Baked
Puddings 156
Sweet Biscuits 154
Milk Puddings 150
Hot Desserts 148
Lamb/Mutton 142 Based on a index where
Cakes/Tarts/Pastries 139 100 is the average
Fresh Seed Vegetables 167
Salad Vegetables 165 Total In Home, Adults 65+, 52 w/e end Aug 2007
66
Figure 6: Top foods consumed by Adults 65+ in volume.
% of Adults 65+ Total Food
Figure 7: Adults 65+ have more cold foods at the Breakfast, Lunch,
Teatime and In Home Snacks occasions. The evening meal occasion is
more about hot food.
% of Total Foods
occasions
Cooked by Adults 65+.
Note: Total adds up to more than 100% as there

may be several meal components at the occasion Total In Home, Adults 65+ 52 w/e Aug 2007
67
List of Tables and Figures
Tables
Table 1 Mortality rates in selected outbreaks of systemic listeriosis
Table 2 Reported deaths amongst non-pregnant listeriosis cases in

Table 3 Food products associated with the transmission of listeriosis

worldwide
Table 4 Numbers of cases with and without underlying illnesses in all

patients 60 years and over
Table 5 Cases and clusters of human listeriosis in England and Wales

1999-2007 with associations with food vehicles
Table 6 Underlying illnesses in listeriosis patients aged 60 years and over:

England and Wales
Table 7 UK Food surveys of listeria contamination in foods, 1997-2007
Table 8 Changes in the rates of L. monocytogenes contamination of

foods examined in England and Wales
Table 9 Examples of food safety advice on listeriosis provided to

vulnerable groups by non-UK authorities
Figures
Fig. 1 Numbers of reported listeriosis cases: England and Wales 1990-2007
Fig. 2 Age specific rates of listeriosis in England and Wales 1990-2006
Fig. 3 Total L. monocytogenes isolations from blood and CSF
Fig. 4 Age group specific rates of human listeriosis in England and Wales
Fig. 5 Net cost of dyspepsia medication, England 1991-99
68
Glossary of Terms and Abbreviations
Terms
Achlorhydria Absence of production of acid in the stomach.
ActA protein Protein expressed by L. monocytogenes involved in

motility of the organism within a host cell.
Acute disease A disease which has rapid onset and lasts for a relatively
short period of time. It can also refer to a very severe
or painful disease.
Amniotic fluid Protecting fluid which fills the amniotic sac which
surrounds the foetus during pregnancy.
Animal model A study using animal(s) that uses conditions similar to

those seen in humans to be representative of what
would occur in the human population.
Antibody Protein found in the blood and other body fluids that
recognises and binds to foreign substances (or antigens).
Antigen A molecule, usually a protein or carbohydrate,

recognised as foreign by the immune system.
Antimetabolite A chemical or drug which interferes with normal

biochemical functions of a cell.
Ascertainment ratio Ratio of the estimation of the numbers of cases of

illness in the population to the numbers reported to
national databases for laboratory confirmed infections.
Asymptomatic Without symptoms.
Atorvastatin Type of statin.
Avirulent Not showing virulence.
aw Water activity the amount of free water in a given

substance (eg food substance). Free water is not the
total water present in a substance, it can vary
depending on other things in the product, for example
the salt and sugar content.
Bacteraemia Presence of bacteria in the bloodstream.
69
B-cell (B lymphocyte) Type of lymphocyte
B-cell lymphoma Type of cancer affecting B lymphocytes
Blood culture Procedure for detecting the presence of an organism in

blood.
Campylobacteriosis Gastro-intestinal infection caused by a member of the

genus Campylobacter. In humans this is usually C. jejuni.
Capecitabine An antimetabolite drug.
Cases Those identified as having a particular condition.
Cellular immune Mechanisms to protect against disease (immunity) at

function the cellular level.
Cerebritis Infection of the brain.
cfu/g Colony forming units per gram a measure of the

numbers of a microorganism within a sample.
CHOP Type of chemotherapy treatment for non-Hodgkins

lymphoma.
CHOP-R Type of chemotherapy treatment for non-Hodgkins

lymphoma containing rituximab.
Chronic condition Long lasting health-related condition.
Chronic lymphocytic Type of cancer affecting white blood cells

leukaemia.
Chronic myeloid Type of cancer affecting white blood cells.

leukaemia
Clostridium difficile Species of Gram positive spore forming bacteria - can

be associated with disease particularly hospital
acquired infections.
Clostridium difficile- Spectrum of disease from mild diarrhoea to life

associated disease -threatening colitis (inflammation of the colon) caused
by C. difficile. Nearly all cases follow treatment with
antibiotics.
Cofactors Required for the activity of an enzyme.

(possibly infections)
Colorectal Involving the colon (large bowel) and rectum.
70
Co-morbidity Disease or condition which exists independently of

another.
Comparator cohort Controls for a cohort study - used to compare to cases.
Continuous A method for removing waste from the blood, as well

ambulatory as excess fluid, when the kidneys are incapable of this
peritoneal dialysis (i.e. in renal failure). Continuous ambulatory peritoneal
dialysis (CAPD), the most common type, needs no
machine and can be done at home. Exchanges of fluid
are done periodically throughout the day.
Contra-indicated To indicate inadvisability, for example the inadvisability

of a medical treatment.
Cumulative risk The risk that an event will occur as time progresses.
Cutaneous lesion Wound of the skin.
Cyclophosphamide Type of drug used to treat cancer.
Cytoplasm The fluid that fills most cells.
Cytoskeletal Of or pertaining to the cytoskeleton - cellular

"scaffolding" or "skeleton" contained within the
cytoplasm.
Cytotoxic treatment Any treatment that is toxic to cells.
Demographic Population characteristics.
Denominator data Lower portion of a fraction used to calculate rate or

ratio - i.e. the population at risk.
Diary based studies Study where participants use a diary as research tool to
record data from individuals.
Disease modifying A class of drugs used to slow the progression of

anti-rheumatic drugs anti-immune diseases.
(DMARDS)
Dyspepsia Indigestion.
Encephalitis Acute inflammation of the brain.
Endocarditis Inflammation of the inner layer of the heart.
Endophthalmitis Inflammation of the inner eye.
Enteric infections Infection of the gut/intestinal system.
71
Enterocolitis Inflammation of the gut/intestines.
Enumeration To count/quantify/define numerically. Enumeration

tests are used to establish the amount of a specific
micro-organism that is present in a sample.
Enzyme A molecule which catalyses (increases the rate) of

chemical reactions.
Epidemiology The study of the occurrence, transmission and control

of disease in a population.
Etanercept A disease-modifying anti-rheumatic drug (DMARD).
Facultative A bacterium which, although capable of independent

intracellular existence, can survive, and in some cases multiply,
bacterium within cells.
Fludaribine Type of chemotherapeutic drug used to treat

haematological malignancies.
Gastric atrophy Condition where stomach muscles become weak and

shrink.
Gastroenteritis Inflammation of gastrointestinal tract.
Gastro-intestinal Digestive tract.
Gene A discrete section of DNA with a specific function. For

example a gene may contain all the DNA to code for a
protein.
Generic Drug sold after the patent for the original formulation
(as applied to has expired.
pharmaceuticals)
Genome All the genetic material for an organism.
Genotypic Relating to genotype the genetic make-up of an

organism.
Genus A level of the biological classification of organisms

based on the fundamental properties of the organisms.
Gestation Carrying an embryo/foetus inside female animal i.e.

during pregnancy.
Gram stain Method of using dyes to categorise bacteria.
H2-receptor Type of drug used to reduce acid production by the

antagonist (H2-RA) stomach.
72
Haematological Type of cancer which affects the blood, bone marrow

malignancy or lymph nodes.
Haemolysin Substance that can cause lysis of red blood cells.
HMG-CoA reductase Enzyme involved in the production of cholesterol
Hepatitis Inflammation of the liver.
Hepatosplenomegaly Enlargement of liver and spleen.
Host-cell A cell that contains foreign molecules, such as viruses,

or bacteria. For example, a cell can be host to a virus.
Imatinib A protein kinase inhibitor.
Immunocompromised Used to describe someone who has an impaired

immune system - usually due to treatment or
underlying illness.
Immunodeficiency See immunocompromised.
Immunomodulatory Adjusting or regulating immune system.
Immunosenescence General decline in the function of the immune system

as an individual ages.
Immunosuppressive Inhibit/prevent immune system action.
Infliximab A monoclonal antibody which may be used as a

disease-modifying anti-rheumatic drug (DMARD)
in vitro In laboratory environment.
in vivo Inside a living organism.
Internalins Cell surface associated proteins which allow

attachment to cells and are involved with viruses being
taken internalised within cells.
Intestinal mobility Ability of gut to move, or ability for things to pass

through the gut.
Intracellular On the inside of a cell.
Isolate Pure culture of bacteria originating from a particular

sample.
L. monocytogenes Enzyme that increases isoprenoid synthesis.

HMG-CoA reductase
Leflunomide A disease-modifying anti-rheumatic drug (DMARD).
73
Listeria Gram-positive pathogenic bacteria that can cause

monocytogenes listeriosis in humans.
Listeriosis A rare but potentially life-threatening disease caused

by Listeria monocytogenes infection. Healthy adults
are likely to experience only mild infection, causing
flu-like symptoms or gastroenteritis. However,
L. monocytogenes infection can occasionally lead to
severe blood poisoning (septicaemia) or meningitis.
Lovastatin Type of statin.
Lymphocyte Type of white blood cell and part of the immune

system.
Malignancy Tumour that can invade and destroy nearby tissue, and
possibly spread to other parts of the body.
Meconium Earliest infant stools.
Meningitic/meningitis Inflammation of the meninges of the brain and the

spinal cord.
Meta-analysis Statistical technique in which the results of several sets

of data from studies examining the same research
question are pooled and subject to further analysis.
Metastatic Spread of cancer beyond the originating tissue or organ.
Meticillin-resistant MRSA A subtype of the Staphylococcus aureus

Staphylococcus aureus bacterial species that is resistant to common types of
antibiotics.
Microflora All the microorganisms in a given environment or

location.
Monoclonal antibody Antibody produced by one type of lymphocyte

derived from a single parent cell. Can be used to target
particular antigens found on cancer cells.
Neonatal Infant in first four weeks after birth.
Non-selective The substance that is used in the laboratory to grow

laboratory media bacteria.
Notifiable disease A disease that must be reported to the competent

authority when diagnosed.
Omeprazole Drug used to reduce stomach acid, in the group known

as protein pump inhibitors.
74
Pathogen Organism able to cause disease/illness.
Peritonitis Inflammation of the membrane lining (peritoneum)

covering the intestinal tract and surrounding the
stomach.
pH A measure of how acidic or alkaline something is. Low

pH is acidic, High pH is alkaline.
Phagocytosis Process whereby cells or microorganisms ingest

particulates.
Phenotype Observable characteristics of an organism.
Phospholipases Enzymes that hydrolyse phospholipids.
Pneumonia Inflammatory illness of the lung.
Polymorphisms Alternatives of the same gene, or part of DNA, within a

species.
Presence/ Common microbiological test to determine whether a

absence test specific microorganism is present without enumeration.
Protein kinase Chemotherapeutic agent which acts by inhibiting

inhibitor protein kinase in rapidly dividing cells.
Proton pump Type of drug used to reduce acid production by the

inhibitor stomach.
Pulsed-field gel Technique used to separate DNA fragments by size.

electrophoresis
Regional microflora Bacteria found in all individuals at particular body sites

(e.g. the large bowel).
Rheumatoid arthritis Long lasting disorder that causes the immune system to
attack the joints, leading to inflammation of the joints
and other organs of the body.
Rillettes A coarse pt-type product
Rituximab A monoclonal antibody used to target B-lymphocytes.
Salmonella Specific type of Salmonella bacteria, full name

Typhimurium Salmonella enterica serovar Typhimurium.
Salmonella spp A genus of gram negative bacteria which can cause

salmonellosis in humans.
Selective media Media that will only allow specific types of bacteria to
grow.
75
Septicaemic Bacteria present in the blood, where symptoms are

seen (blood poisoning).
Serotyping A method of distinguishing types of bacteria

(serotypes) within a single species by defining their
antigenic properties (see antigen) on the basis of their
reaction to known antisera.
Statin (or HMG-CoA Type of medication used to lower blood levels of

reductase inhibitor) cholesterol.
Steroids A group of hormones that occur naturally in the body

and medications based on them.
Strain A population of organisms within a species or sub-

species distinguished by typing.
Subclinical Infection which does not show symptoms, or before

the symptoms appear.
Symptomatic Displaying symptoms of a disease.
Systemic Throughout the whole body.
T-lymphocyte Type of lymphocyte.
Tegafur An antimetabolite drug.
Th1 Type of T lymphocyte involved in directing other cells

of the immune system.
Thymic involution Shrinking of the thymus gland with ageing. The thymus
is an important organ for maturation of T-lymphocytes.
Typing Any method used to distinguish between closely

related organisms.
Varicella zoster virus Virus in the herpes family that causes chickenpox and
shingles.
Virulence The capacity of a microorganism to cause disease.
Virulence attributes Characteristics of bacteria microorganism that allow it

to cause disease.
White blood White blood cells form part of the immune system, so
cell count the white blood cell count indicates how well the
immune system is functioning.
76
Abbreviations
BRC British Retail Consortium
CNS Central Nervous System
CSF Cerebrospinal fluid
DMARD Disease modifying anti-rheumatic drug
EFSA European Food Safety Authority
GELA study Groupe d'Etude des Lymphomes de l'Adulte study
HPA Health Protection Agency
MRSA Meticillin-resistant Staphylococcus aureus
MRC CLL4 trial Medical Research Council Chronic Lymphocytic

Leukaemia Trial 4
PFGE Pulsed-field gel electrophoresis
AFLP Amplified fragment length polymorphism
CML Chronic myeloid leukaemia
NICE National Institute for Health and Clinical Excellence
GI Gastro-intestinal
PPI Proton pump inhibitor
CIG Geriatric Index of Co-morbidity
H2RA H2 receptor antagonist
RTE Ready-to-eat
TNS A market research company
CLL Chronic lymphocytic leukaemia
77
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July 2009 Microbiological Safety of Food
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ACMSF A3 Listeria Elderly:ACMSF A3 cover 27/7/09 9:32 PM Page 1

Advisory Committee on the

Ad Hoc Group on Vulnerable Groups

Report on the Increased Incidence

Further copies of this publication can be downloaded from: acmsf.food.gov.uk/acmsfreps/

Ad Hoc Group on Vulnerable Groups

Report on the Increased Incidence

Advises the Food Standards Agency on the

Non-behavioural factors which may increase 4.21

1. In this report the Ad Hoc Group has considered the change in

2. This report follows information from the Health Protection Agency to

3. In June 2007 ACMSF referred this issue to its Ad Hoc Group on

5. Key conclusions and recommendations arising from the work of the

The majority of cases of human listeriosis appear to be sporadic

The increase and shift in presentation of listeriosis cannot be

Elderly individuals are more likely to have underlying conditions

and data collection should be conducted to identify which

Maintaining active surveillance for Listeria spp. in foods is

Data on shopping and food behaviour and consumption patterns

growth of L. monocytogenes in foods. The Committee also

The organism has been found in chilled ready-to-eat foods at a

Definition of a vulnerable group

8. Although risk factors for listeriosis are well documented, identification

9. A definition of a vulnerable group, such as the elderly, is necessary if

1 NHS Direct web site: http://www.nhs.uk/conditions/Listeriosis/Pages/Introduction.aspx

The ACMSFs approach to its work

Chapter 2: Hazard identification and

2.1 Listeria is a genus of Gram-positive bacteria and comprises six species:

Table 1: Mortality rates in selected outbreaks of systemic listeriosis

Listeriosis in non-pregnant individuals

Table 2: Reported deaths amongst non-pregnant listeriosis cases in

Source: HPA unpublished data

2.15 L. monocytogenes is a facultative intracellular pathogen, and multiple

Epidemiology of listeriosis and changing pattern of human

Table 3. Food products associated with the transmission of listeriosis

Dairy Meats Fish Vegetables Complex

Fig. 1. Numbers of reported listeriosis cases:

Fig. 2. Age specific rates of listeriosis in England and Wales 1990-2006

Fig. 3. Total L. monocytogenes isolations from blood and CSF

Fig. 4. Age group specific rates of human listeriosis in England

Table 4. Numbers of cases with and without underlying illnesses in all

Year Region Cases Vehicle

Source: Gillespie et al 2006 and HPA unpublished data

2.21 A similar change in incidence of listeriosis has been reported in Scotland

2.23 Consumption of contaminated food is believed to be the principal

2.24 The majority of cases are/appear to be sporadic and foods associated

2.26 A similar change in presentation of listeriosis has been reported in

2.28 Studies should be undertaken to develop methods for screening

Chapter 3: Report rationale

Our four main hypotheses

1. The rise in cases of listeriosis in immunocompromised people over

2. The population predominantly affected by the recent increase has

3. The pathogen, L. monocytogenes has become more virulent and

4. Levels of exposure have increased.

(1) The rise in cases of listeriosis in immunocompromised people over

3.2 We considered the possibility that the recent rises in listeriosis in

(2) The population predominantly affected by the recent increase has

(3) The pathogen, L. monocytogenes has become more virulent and

(4) Levels of exposure have increased

3.6 These hypotheses will be considered in the following chapter.

Chapter 4: Consideration of key hypotheses

Hypothesis 1: The rise in cases of listeriosis in

4.3 Improvements in laboratory methods (especially in the isolation of